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Genetic relatedness in groups is sex‐specific and declines with age of helpers in a cooperatively breeding cichlid
Abstract
Kin selection can explain the evolution of cooperative breeding and the distribution of relatives within a population may influence the benefits of cooperative behaviour. We provide genetic data on relatedness in the cooperatively breeding cichlid Neolamprologus pulcher. Helper to breeder relatedness decreased steeply with increasing helper age, particularly to the breeding males. Helper to helper relatedness was age-assortative and also declined with age. These patterns of relatedness could be attributed to territory take-overs by outsiders when breeders had disappeared (more in breeding males), between-group dispersal of helpers and reproductive parasitism. In six of 31 groups females inherited the breeding position of their mother or sister. These matrilines were more likely to occur in large groups. We conclude that the relative fitness benefits of helping gained through kin selection vs. those gained through direct selection depend on helper age and sex.
... (c) Finally, N. pulcher groups consist of a mixture of related and unrelated individuals. Relatedness to breeders declines with helper age, so that large adult helpers, which are most efficient in providing help, are usually unrelated to the breeder's offspring and beneficiaries of help (Dierkes et al., 2005). Opposite to cooperative systems driven by kin selection, but in accordance with the pay-to-stay mechanism, in N. pulcher relatedness reduces cooperative effort (Zöttl et al., 2013b). ...
... The group augmentation hypothesis (Woolfenden 1975;Rood 1978;Brown 1987;Kokko et al. 2001a) states that if helpers in cooperatively breeding animals raise the reproductive success of the group, the benefits of living in a resulting larger group favor the evolution of helping behavior. Kingma et al. (2014) illustrated that direct benefits of group augmentation can accrue via different evolutionary mechanisms that relate closely to well-supported general concepts of group living and cooperation (Kokko et al. 2001a;Dierkes et al. 2005;Bergmüller et al. 2007;Clutton-Brock 2009a;Heg & Taborsky 2010;Sumner et al. 2010;Kingma et al. 2011;Wong & Balshine 2011;Zöttl et al. 2013a). ...
... Subordinates can inherit dominance if they outlive those above them in the hierarchy (Strassmann & Meyer 1983;Wiley & Rabenold 1984;Field et al. 1999Field et al. , 2006Monnin & Peeters 1999;Monnin & Ratnieks 1999;Cant & Field 2001). In many cooperative breeders, a proportion of helpers can inherit their home territory (Woolfenden 1975;Rood 1978Rood , 1990Wiley & Rabenold 1984;Dierkes et al. 2005;Hawn et al. 2007;Field & Cant 2009;Sumner et al. 2010;Kingma et al. 2011Kingma et al. , 2014Leadbeater et al. 2011;Sharp & Clutton-Brock 2011;Marino et al. 2012). Ragsdale (1999) defined the resource inheritance, a form of future direct benefit, as the probability of inheriting valuable resources multiplied by the expected number of offspring that an individual would produce after it inherits the resources (relative to a lone breeder). ...
... These helpers may gain direct fitness benefits, either by sharing in reproduction with the breeders (Awata et al. 2005(Awata et al. , 2006aRiehl 2013) or by increasing their future reproductive success (Komdeur 1996;Hatchwell et al. 1999;Kingma et al. 2021). The latter might be achieved by inheriting dominant territories (Goldizen et al. 2002;Kokko and Ekman 2002;Dierkes et al. 2005;Stiver et al. 2006;Josi et al. 2021a, b), increased survival by living in large groups (group augmentation (Clutton-Brock et al. 1999;Kingma et al. 2014)), gaining access to resources as payment (payto-stay (Gaston 1978;Mulder and Langmore 1993;Russell et al. 2008)), or enhancing their prestige within the group (signal of prestige (Bergmüller et al. 2007;Wong and Balshine 2011)). Depending on the ecological setting, the number of related and unrelated helpers may furthermore vary within and between species (Painter et al. 2000;Griffin et al. 2003;Nichols et al. 2012;Rubenstein 2016;Tanaka et al. 2016). ...
... There is much less observational evidence of dispersal in cooperatively breeding cichlids (but see Josi et al. 2021a), because of the difficulty in long-term continuous tracking of small fish in the field. Instead, genetic analysis of relatedness is used to estimate dispersal patterns of helpers (Dierkes et al. 2005). In N. pulcher, DNA analysis showed that female helpers dispersed shorter distances and more often than male helpers (Hellmann et al. 2016). ...
... The number of individuals and percentages in parentheses are shown in bars sexes were immature. This suggests that juveniles delay dispersal and become helpers, as is known to occur for other cooperatively breeding cichlids, such as N. pulcher (Dierkes et al. 2005), N. savoryi (Josi et al. 2021b), and N. obscurus (Tanaka et al. 2015). Because individuals of N. meeli occupied all available snail shells in the study area, dispersal to vacant exposed snail shells is not possible. ...
Cooperative breeding systems, where individuals other than parents assist in raising offspring, have been documented in insects, fish, birds, and mammals. Still, the factors driving the evolution of such complex systems are not fully understood. Here, we report a new example of cooperative breeding in the obligate shell-brooding cichlid fish Neolamprologus meeli from Lake Tanganyika. Field observations revealed that dominant males were either monogamous or polygynous, with each mating with one to four dominant females. Dominant females maintain nests containing one to ten empty gastropod shells used as breeding substrates and shelters. Up to four immature subordinates of either sex lived in these nests. They assisted with territory defense and nest maintenance, the frequency of which was not different from that of the dominants. Parentage analyses showed that most subordinates were the offspring of at least one of the breeders, suggesting that juveniles delay dispersal and help in raising their relatives. The relatedness of subordinates to the breeders declined with increasing body size and was significantly higher to female than to male breeders. These patterns could be caused by extra-pair paternity, between-group dispersal of helpers, or sex differences in breeder turnover. Male helpers were larger than female helpers, and six out of eight dispersed individuals were females, suggesting female-biased dispersal. Because N. meeli is phylogenetically distinct from other cooperatively breeding cichlids, these results contribute to a better understanding of cooperative breeding in fishes and to understanding of the evolution of complex social systems in general.
Significance statement
Cooperatively breeding cichlid fishes of Lake Tanganyika are an excellent model for studying the evolution of social complexity because cooperative breeding evolved at least 5–6 times independently in a small phylogenetic group. Here, we provide a new example of cooperative breeding in the cichlid Neolamprologus meeli. Field observations revealed that these fish were either monogamous or polygynous. Subordinates remained in the breeders’ nests and helped with territory defense and nest maintenance. Subordinates of both sexes were unlikely to participate in reproduction because of their immature gonads. Parentage analyses showed that most helpers and juveniles were offspring of the dominant breeders, suggesting that N. meeli has a kin-structured cooperative breeding system. As N. meeli is phylogenetically distinct from all other cooperatively breeding cichlids, these results pose a hitherto undescribed independent evolutionary event, leading to a highly complex social system.
... Kin selection can explain alloparental care because of fitness benefits accrued to related individuals (4,5), and genetic relatedness among group members is indeed a good predictor of evolutionary transitions to cooperative breeding (6)(7)(8). However, in many cases, the group members are not related to each other (9)(10)(11)(12). Notably, group living as a result of limited dispersal may bear inevitable direct fitness benefits that can also select for philopatry and helping (13)(14)(15)(16). ...
... Our results indicate that individuals staying in their natal territory should decrease help over time as the degree of relatedness between them and the young declines with their own age due to time-dependent breeder replacement and dispersal dynamics (Fig. 3, top left) (9). Reduced helping levels with low relatedness have been observed in several cooperative breeders (52). ...
... The emergence of helping after group formation can result from both group augmentation benefits and kin selection. Direct and mutual fitness benefits from increased group size as a driver of cooperation can explain puzzling phenomena like the "kidnapping" of members from other groups observed in several species (40,61) or the presence of unrelated helpers within groups (9,12). ...
The evolution of cooperative breeding has been traditionally attributed to the effect of kin selection. While there is increasing empirical evidence that direct fitness benefits are relevant, the relative importance of alternative selection mechanisms is largely obscure. Here, we model the coevolution of the cornerstones of cooperative breeding, delayed dispersal, and alloparental care, across different ecological scenarios while allowing individuals to adjust philopatry and helping levels. Our results suggest that (i) direct fitness benefits from grouping are the main driver for the evolution of philopatry; (ii) kin selection is mainly responsible for the emergence of alloparental care, but group augmentation can be a sufficient promoter in harsh environments; (iii) the coevolution of philopatry and alloparental care is subject to positive feedback; and (iv) age-dependent dispersal is triggered by both group benefits and relatedness. Model predictions are supported by empirical data and provide good opportunities for comparative analyses and experimental tests of causality.
... Although the social systems of cooperatively breeding cichlids seem to have much in common, the mechanisms that shape and maintain these systems strongly differ between species. For instance, in N. pulcher, genetic relatedness between breeders and subordinates decreases with increasing subordinate body size, so that large subordinates are usually unrelated to the breeders (Dierkes et al., 2005). Similar patterns also occur in N. savoryi (Josi, Heg, et al., 2021), whereas N. obscurus and N. multifasciatus subordinates appear to be more closely related to the breeders they assist (Taborsky, 2009;Tanaka et al., 2015). ...
... While large N. pulcher and N. savoryi subordinates might participate in reproductive events, reproduction is highly skewed towards dominants (Dierkes et al., 2005;Josi, Heg, et al., 2021). In contrast, breeding nests of Julidochromis ornatus are cooperatively cared for by a few non-kin subordinate males that gain opportunities to sire the brood with the female breeder by contributing to parental care, reducing the intensity of the reproductive skew (Awata et al., 2005(Awata et al., , 2006(Awata et al., , 2010. ...
... We found solitary individuals near the breeding nests of N. bifasciatus. Young individuals of the cooperatively breeding cichlid N. pulcher occasionally migrate into nearby groups, where they become subordinates (Dierkes et al., 2005;Stiver et al., 2004), often visiting the group spontaneously before immigration (Bergmüller et al., 2005). Such regular visits allow individuals to gain familiarity and develop social relationships with nearby groups (Bergmüller et al., 2005;Jungwirth et al., 2015). ...
Cooperative breeding, a social system in which offspring receive care from other group members as well as their parents, occurs in insects, fish, birds and mammals. In this study, we report a new example of cooperative breeding in the cichlid fish (Neolamprologus bifasciatus). This species, endemic to Lake Tanganyika, Africa, inhabits rocky areas at depths below 30 m. Observations of eight nests using underwater video cameras showed that one to six subordinates were present in the nests of breeding pairs. The subordinates shared shelters with juveniles and breeders and engaged in brood/territorial defence and nest maintenance (removing sand from the nest), albeit at a lower frequency than female breeders. The frequency of sand digging by subordinates and female breeders decreased as the number of subordinates in the group increased, suggesting that subordinates reduce the costs of nest maintenance for breeders. The male breeders seldom showed territorial defence and nest maintenance. Subordinates exhibited submissive behaviours towards dominant breeders and larger subordinates within their breeding group, indicating a dominance hierarchy among group members. Gonad examination revealed that the subordinates of both sexes were sexually immature, suggesting that they may not participate in reproduction. An aquarium experiment showed that juveniles become subordinates in their natal nest and participate in territory defence. We conclude that N. bifasciatus is a cooperative breeder, with social systems and subordinate roles similar to those observed in other cooperatively breeding cichlids.
... In fishes, cooperative breeding has been described for approximately 25 lamprologine cichlids endemic to Lake Tanganyika (Taborsky 1994;, where it evolved several times independently (Dey et al. 2017;Tanaka et al. 2018b;Ronco et al. 2021). Notably, the cooperatively breeding species in this clade vary greatly in within-group relatedness levels, ranging from species where most helpers are unrelated to the breeders they support, to others where subordinates usually help their own parents (Awata et al. 2005;Dierkes et al. 2005;Tanaka et al. 2015). For example, large helpers of N. pulcher are often unre-lated to the breeders they aid Stiver et al. 2005), whereas helpers of Neolamprologus obscurus are typically closely related to the breeders they assist (Tanaka et al. 2015). ...
... We used the Blumberg growth curve of Skubic et al. (2004) to estimate the age (in days) of each individual in the respective population (cf. Dierkes et al. 2005). Growth rates at KS are comparable to the KK population (Josi et al. 2021). ...
... The pairwise genetic relatedness between breeder males and their helpers within the group, as well as the relatedness of breeder females to their helpers in their subgroup, were set as response variables. Helper body size (ln[SL]) was set as a continuous effect and breeder sex as a fixed effect (see also Dierkes et al. 2005). The same analysis was performed on a subset of sexed helpers, that is, by adding helper sex as a fixed effect (excluding n = 120 out of 954 comparisons of helper to breeder relatedness due to uncertain sexing of helpers). ...
Kin selection plays a major role in the evolution of cooperative systems. However, many social species exhibit complex within-group relatedness structures, where kin selection alone cannot explain the occurrence of cooperative behaviour. Understanding such social structures is crucial to elucidate the evolution and maintenance of multi-layered cooperative societies. In lamprologine cichlids, intragroup relatedness seems to correlate positively with reproductive skew, suggesting that in this clade dominants tend to provide reproductive concessions to unrelated subordinates to secure their participation in brood care. We investigate how patterns of within-group relatedness covary with direct and indirect fitness benefits of cooperation in a highly social vertebrate, the cooperatively breeding, polygynous lamprologine cichlid Neolamprologus savoryi. Behavioural and genetic data from 43 groups containing 578 individuals show that groups are socially and genetically structured into subgroups. About 17% of group members were unrelated immigrants, and average relatedness between breeders and brood care helpers declined with helper age due to group membership dynamics. Hence the relative importance of direct and indirect fitness benefits of cooperation depends on helper age. Our findings highlight how both direct and indirect fitness benefits of cooperation and group membership can select for cooperative behaviour in societies comprising complex social and relatedness structures.
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... The multi-male/multi-female category described in Heg and Bachar (2006), which has been referred to by Tanaka et al. (2018), denotes groups consisting of multiple sexually mature males and females. To what extent these adult subordinates gain reproductive share is known from 6 cooperatively breeding cichlids for which genetic data are available (Neolamprologus pulcher, N. savoryi, N. obscurus, N. multifasciatus, Julidochromis ornatus, J. transcriptus;see Kohler, 1998;Awata, Munehara, & Kohda, 2005;Dierkes, Heg, Taborsky, Skubic, & Achmann, 2005;Kohda et al., 2009;Tanaka et al., 2015;Hellmann et al., 2016;Heg et al. in revision; see Taborsky, 2009Taborsky, , 2016. Without exception, all these studies revealed that groups in the respective species contain larvae, young or helpers of different degrees of relatedness to the breeders, revealing that they are genetically non-monogamous. ...
... Regarding mating patterns, what really matters to comprehend the role of direct and indirect benefits in the evolution of cooperative breeding is the degree of relatedness between helpers and the breeders' offspring. Even if breeders are generally monogamous, changes in breeder identity due to frequent deaths or turnovers in territory ownership lead to reduced relatedness between existing helpers and new offspring (Taborsky & Limberger, 1981), as has been shown in N. pulcher (Dierkes et al., 2005). Additionally, immigration, which occurs regularly in the cooperatively breeding cichlids investigated thus far (see Taborsky, 2016 for review), significantly reduces relatedness between helpers and beneficiaries. ...
... Additionally, immigration, which occurs regularly in the cooperatively breeding cichlids investigated thus far (see Taborsky, 2016 for review), significantly reduces relatedness between helpers and beneficiaries. Consequently, in the cooperatively breeding cichlids for which genetic data are available, the mean within-group relatedness values are clearly below 0.5 (Awata et al., 2005;Dierkes et al., 2005;Kohler, 1998;Taborsky, 2009;Tanaka et al., 2015), varying with age and size of the subordinates (Dierkes et al., 2005). Dey et al. (2019) state that the alternative phylogenetic trees presented in Tanaka et al. (2018) also suggest 4-5 transitions to cooperative breeding. ...
... But both experiments were conducted using laboratory-reared fish that experienced simplified social settings and were regularly provided high-quality food. It is likely that the heightened complexity observed in the natural environment of N. pulcher-where food acquisition (mostly zooplankton; Gashagaza and Nagoshi 1986) is more challenging, group membership is more dynamic (Dierkes et al. 2005;Fitzpatrick et al. 2008;Jordan et al. 2010;Stiver et al. 2006) and individuals routinely interact with groupmates, neighbours, and heterospecifics (Bergmüller et al. 2005;Desjardins et al. 2008b;Jungwirth et al. 2015aJungwirth et al. , 2015b)-forces individuals to pay greater attention to all forms of social signals, including colour-based signals. A c c e p t e d M a n u s c r i p t ...
... Subordinates, in particular, benefit from having strong affiliative relationships with their groupmates because a well connected subordinate is less likely to be in conflict with other group members and will have relatively low risk of being exiled and losing the protection of the social group (Taborsky 2016(Taborsky , 1984. Moreover, subordinates that are well connected can benefit further because dominants may be more likely to allow them to reproduce Heg et al. 2009;Heg and Hamilton 2008) and may also be more likely to eventually assume the dominant position in their group (Dierkes et al. 2005;Fitzpatrick et al. 2008;Stiver et al. 2006). We therefore predicted that individuals with larger patches would receive more affiliative acts from their groupmates, and more specifically, that this relationship would be strongest among subordinates. ...
Many animals use colour to signal their quality and/or behavioural motivations. Colourful signals have been well studied in the contexts of competition and mate choice, however, the role of these signals in non-sexual, affiliative relationships is not as well understood. Here, we used wild social groups of the cichlid fish Neolamprologus pulcher to investigate whether the size of a brightly coloured facial patch was related to i) individual quality, ii) social dominance, and/or iii) affiliative relationships. Individuals with larger patches spent more time foraging and tended to perform more aggressive acts against conspecific territory intruders. We did not find any evidence that the size of these yellow patches was related to social rank or body size, but dominant males tended to have larger patches than dominant females. Additionally, patch size had a rank-specific relationship with the number of affiliative interactions that individuals engaged in. Dominant males with large patches received fewer affiliative acts from their groupmates compared to dominant males with small patches. However, subordinates with large patches tended to receive more affiliative acts from their groupmates while performing fewer affiliative acts themselves. Taken together, our results suggest that patch size reflects interindividual variation in foraging effort in this cichlid fish and offer some of the first evidence that colourful signals may shape affiliative relationships within wild social groups.
... In addition, helpers prefer to join a group instead of breeding independently [13], and they prefer to join larger versus smaller groups despite thereby reducing their chance of inheriting the territory owing to joining a longer queue for the breeding position [14,15]. Furthermore, helpers increase the reproductive output of breeders [16,17], which yields larger groups since most offspring remain philopatric for a long time [18][19][20]. All this suggests that the preconditions for the evolution of alloparental care by group augmentation are met in this species. ...
... Neolamprologus pulcher is a cooperatively breeding cichlid endemic to Lake Tanganyika, East Africa [21]. Breeding groups consist of a dominant breeding pair that largely monopolizes reproduction, and 0-20 related and unrelated helpers [11,12,18,22,23]. Groups typically use self-dug burrows under rocks, and small holes and crevices as shelters and for breeding [12,19]. ...
Mechanisms selecting for the evolution of cooperative breeding are hotly debated. While kin selection theory has been the central paradigm to explain the seemingly altruistic behaviour of non-reproducing helpers, it is increasingly recognized that direct fitness benefits may be highly relevant. The group augmentation hypothesis proposes that alloparental care may evolve to enhance group size when larger groups yield increased survival and/or reproductive success. However, there is a lack of empirical tests. Here we use the cooperatively breeding cichlid fish Neolamprologus pulcher, in which group size predicts survival and group stability, to test this hypothesis experimentally by prompting two cooperative tasks: defence against an egg predator and digging out sand from the breeding shelter. We controlled for alternative mechanisms such as kin selection, load lightening and coercion. As predicted by the group augmentation hypothesis, helpers increased defence against an egg predator in small compared with large groups. This difference was only evident in large helpers owing to size-specific task specialization. Furthermore, helpers showed more digging effort in the breeding chamber compared with alternative personal shelters, indicating that digging is an altruistic service to the dominant breeders.
... For example, in work on wild populations of killer whales that show bisexual philopatry, we have found a strong match with the theoretical prediction of increasing female relatedness with age (figures 1c and 2a(iii)) [16]. Analogous patterns have been found in several species of cooperative breeders where relatedness of an individual to the local group changes as a function of age [42][43][44]. For example, in African wild dogs (Lycaon pictus), dwarf mongooses (Helogale parvula) and Lake Tanganyika cichlids (Neolamprologus pulcher) the relatedness of non-breeding helpers to the dominant breeders decreases with helper age due to a combination of breeder turnover, extra-pair paternity and helper immigration [42][43][44]. ...
... Analogous patterns have been found in several species of cooperative breeders where relatedness of an individual to the local group changes as a function of age [42][43][44]. For example, in African wild dogs (Lycaon pictus), dwarf mongooses (Helogale parvula) and Lake Tanganyika cichlids (Neolamprologus pulcher) the relatedness of non-breeding helpers to the dominant breeders decreases with helper age due to a combination of breeder turnover, extra-pair paternity and helper immigration [42][43][44]. ...
Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.
... Strong affiliative relationships with groupmates can improve an individual's social rank and fitness (Schülke et al., 2010;Silk et al., 2003;Strauss and Holekamp, 2019). In N. pulcher, affiliative relationships are likely more important to females because they are less likely to disperse than are males (Hellmann et al., 2016;Stiver et al., 2007) and often ascend to dominant breeder status from within their social group (Dierkes et al., 2005;Stiver et al., 2006). We found that subordinate females performed twice as many affiliative acts as subordinate males, supporting the notion that affiliative relationships are important to female N. pulcher; potentially as a mechanism to enhance their social standing within the group. ...
... For example, exposure to either a predator or novel conspecific resulted in acutely elevated cortisol levels in three-spined sticklebacks (Gasterosteus aculeatus), but levels of monoamines in regions of the brain involved in regulating glucocorticoid synthesis (hypothalamus, reticular formation, and telencephalon) showed stressorspecific responses suggesting that different neural regulatory mechanisms are involved (Bell et al., 2007). N. pulcher are routinely exposed to a diverse set of challenges that require unique behavioural, physiological, and cognitive responses, including predator attacks (Groenewoud et al., 2016;Heg et al., 2004;Jungwirth et al., 2015), territory disputes with neighbours (Frostman and Sherman, 2004;Saeki et al., 2018), and changes in the composition of their social group (Culbert et al., 2018;Dierkes et al., 2005;Fitzpatrick et al., 2008;Stiver et al., 2006). While each of these challenges is likely to activate the HPI axis and cause elevated glucocorticoid synthesis, the neurohormonal changes that facilitate HPI axis activation may vary owing to the unique responses required to overcome different challenges. ...
Individuals often respond to social disturbances by increasing prosociality, which can strengthen social bonds, buffer against stress, and promote overall group cohesion. Given their importance in mediating stress responses, glucocorticoids have received considerable attention as potential proximate regulators of prosocial behaviour during disturbances. However, previous investigations have largely focused on mammals and our understanding of the potential prosocial effects of glucocorticoids across vertebrates more broadly is still lacking. Here, we assessed whether experimentally elevated glucocorticoid levels (simulating endogenous cortisol responses mounted following disturbances) promote prosocial behaviours in wild groups of the cichlid fish, Neolamprologus pulcher. Using SCUBA in Lake Tanganyika, we observed how subordinate group members adjusted affiliation, helping, and submission (all forms of prosocial behaviour) following underwater injections of either cortisol or saline. Cortisol treatment reduced affiliative behaviours-but only in females-suggesting that glucocorticoids may reduce overall prosociality. Fish with elevated glucocorticoid levels did not increase performance of submission or helping behaviours. Taken together, our results do not support a role for glucocorticoids in promoting prosocial behaviour in this species and emphasize the complexity of the proximate mechanisms that underlie prosociality.
... Groups defend a number of shelters dug out from sand under rocks, and aggregate in colonies of up to 200 groups [62,63]. Relatedness among group members declines with their age [29], and reproduction is largely monopolized by the breeding pair [31,38]. ...
... 7: 191808 possible appeasing effect on dominant breeders. They occasionally participate in reproduction [38,42,43,83] and may inherit the territory later [29,86]. They might, therefore, benefit from deterring egg predators from the area. ...
Coercion is an important but underrated component in the evolution of cooperative behaviour. According to the pay-to-stay hypothesis of cooperative breeding, subordinates trade alloparental care for the concession to stay in the group. Punishment of idle subordinates is a key prediction of this hypothesis, which has received some experimental scrutiny. However, previous studies neither allowed separating between punishment and effects of disruption of social dynamics, nor did they differentiate between different helping behaviours that may reflect either mutualistic or reciprocal interaction dynamics. In the cooperative breeder Neolamprologus pulcher, we experimentally engineered the ability of subordinates to contribute to alloparental care by manipulating two different helping behaviours independently from one another in a full factorial design. We recorded the treatment effects on breeder aggression, subordinate helping efforts and submissive displays. We found two divergent regulatory mechanisms of cooperation, dependent on behavioural function. Experimental impediment of territory maintenance of subordinates triggered punishment by dominants, whereas prevented defence against egg predators released a compensatory response of subordinates without any enforcement, suggesting pre-emptive appeasement. These effects occurred independently of one another. Apparently, in the complex negotiation process among members of cooperative groups, behaviours fulfilling different functions may be regulated by divergent interaction mechanisms.
... We measured the cooperative actions of members of experimental dyads regarding territory maintenance, i.e., removal of sand from a common shelter, and defense against a predatory fish. In this species, groups of related and unrelated fish exhibit high levels of collaboration and division of labor (Taborsky and Limberger, 1981;Dierkes et al., 2005;Stiver et al., 2005;Bruintjes and Taborsky, 2011;Taborsky, 2016). The dominant individuals in a group largely monopolize reproduction, while subordinates share in all duties of parental care and territory maintenance, including direct egg care, the removal of sand from shelters, and the defense of the territory against predators and competitors (Taborsky and Limberger, 1981;Taborsky, 1984;Taborsky and Grantner, 1998;Bruintjes and Taborsky, 2011;Jungwirth et al., 2015). ...
... These helpers actively engage in territory maintenance, territory defense and brood care (Taborsky and Limberger, 1981;Taborsky, 1984;Bruintjes and Taborsky, 2011). Due to high predation pressure there is a high breeder turn-over in N. pulcher, which means that large helpers often care for non-kin broods (Taborsky and Limberger, 1981;Taborsky, 1984;Brouwer et al., 2005;Dierkes et al., 2005;Stiver et al., 2005). ...
Members of social groups often temporally coordinate their behaviors, for instance in defense or foraging. In the context of cooperation, simultaneous or sequential coordination of behavior may allow social partners to adjust their cooperative effort quickly among each other. By manipulating individual behaviors, here we tested experimentally whether unrelated brood care helpers of the cichlid fish Neolamprologus pulcher would cooperate in dyads when enabled to dig out a joint shelter or to defend their territory against a predator. Both the digging and defense efforts of social partners were contingent on each other's investment, and the test subjects temporally coordinated these behaviors. Remarkably, the direction of conditional responses to each other's cooperative investment diverged between the two chosen experimental time frames, which tested for coaction and reciprocity. Test subjects reduced their own digging and defense efforts while their partners were showing these behaviors themselves, implying that they did not exert coaction but rather economized on their investment. In contrast, if a social partner had helped to dig out the common shelter in a previous time period, focal test fish advanced their digging effort in the subsequent experimental phase, which indicates reciprocal cooperation. Social partners also coordinated shelter use when they could see each other, especially after they had been visually exposed to a predator. Our results reveal coordination of cooperative behaviors among unrelated social partners, which has not yet been experimentally demonstrated in cooperatively breeding vertebrates.
... Although traditionally mainly indirect benefits have been considered to explain cooperative behavior, it becomes increasingly clear that mechanisms increasing the direct fitness of helpers may also be important (Kokko et al. 2001;Dierkes et al. 2005;Bergmüller et al. 2007;Clutton-Brock 2009;Heg & Taborsky 2010;Sumner et al. 2010;Kingma et al. 2011;Wong & Balshine 2011;Zöttl et al. 2013;Kingma et al. 2014, from whom I have taken this paragraph). A frequently suggested mechanism underlying such direct benefits is described by the group augmentation hypothesis, which proposes that helpers gain fitness benefits by enhancing group size if the recruits that are produced as a result of helping behavior in turn increase the survival and/or reproduction of helpers (Woolfenden 1975;Rood 1978;Wiley & Rabenold 1984;Kokko et al. 2001;Heg et al. 2005;Bergmüller et al. 2007;Clutton-Brock 2009;Kingma et al. 2011Kingma et al. , 2014. ...
... We used intermittent flow respirometry to measure resting, routine and maximum metabolic rates (oxygen consumption) of paired dominant and subordinate female N. pulcher from the same social group. We focused on females because affiliative relationships are stronger in female versus male N. pulcher [28] and compared with males, females are more likely to assume a dominant position within their natal group [29,30]. Dominants and subordinates were placed in adjacent respirometry chambers where they could either visually interact (separated by transparent chamber walls) or not (separated by an opaque barrier). ...
Social interactions can sometimes be a source of stress, but social companions can also ameliorate and buffer against stress. Stress and metabolism are closely linked, but the degree to which social companions modulate metabolic responses during stressful situations—and whether such effects differ depending on social rank—is poorly understood. To investigate this question, we studied Neolamprologus pulcher, a group-living cichlid fish endemic to Lake Tanganyika and measured the metabolic responses of dominant and subordinate individuals when they were either visible or concealed from one another. When individuals could see each other, subordinates had lower maximum metabolic rates and tended to take longer to recover following an exhaustive chase compared with dominants. In contrast, metabolic responses of dominants and subordinates did not differ when individuals could not see one another. These findings suggest that the presence of a dominant individual has negative metabolic consequences for subordinates, even in stable social groups with strong prosocial relationships.
... 9, 82,90,104,140 Overall relatedness between subordinates and dominants is low and decreases with helper age, mainly due to the replacement of the breeders. 141,142 Both related and unrelated subordinates participate in brood care of the dominants' broods by cleaning and fanning the eggs, 67,75 digging out sand from the breeding chamber, 138,143 and defending the territory against predators of eggs and young. 7,49,50,54, 75,132,138,139 Individual and kin recognition have been demonstrated in this species. ...
In cooperative societies, group members typically exchange different commodities among each other, which involves an incessant negotiation process. How is the conflict of fitness interests resolved in this continual bargaining process between unequal partners, so that maintaining the cooperative interaction is the best option for all parties involved? Theory predicts that relatedness between group members may alleviate the conflict of fitness interests, thereby promoting the evolution of cooperation. To evaluate the relative importance of relatedness and direct fitness effects in the negotiation process, we experimentally manipulated both the relatedness and mutual behavioural responses of dominant breeders and subordinate helpers in the cooperatively breeding cichlid fish Neolamprologus pulcher. Results show that coercion by breeders is crucial for the performance of alloparental egg care by helpers, but that kinship significantly decreases the need for coercion as predicted by theory. This illustrates the relative importance of kinship and enforcement in the bargaining process.
... In nature, social groups are typically composed of a dominant breeding pair and subordinate helpers of various sizes and sexes [26,27]. Subordinate helpers can be related or unrelated to the breeders [34]. Helping behaviour includes alloparental care, territory defence and territory maintenance [26,35]. ...
Social competence—defined as the ability to optimize social behaviour according to available social information—can be influenced by the social environment experienced in early life. In cooperatively breeding vertebrates, the current group size influences behavioural phenotypes, but it is not known whether the group size experienced in early life influences behavioural phenotypes generally or social competence specifically. We tested whether being reared in large versus small groups for the first two months of life affects social behaviours, and associated life-history traits, in the cooperatively breeding cichlid Neolamprologus pulcher between the ages of four and twelve months. As we predicted, fish raised in larger and more complex groups showed higher social competence later in life. This was shown in several ways: they exhibited more, and earlier, submissive behaviour in response to aggression from a dominant conspecific, and—in comparison to fish raised in small groups—they exhibited more flexibility in the expression of submissive behaviour. By contrast, there was no evidence that early social complexity, as captured by the group size, affects aggression or exploration behaviour nor did it influence the propensity to disperse or show helping behaviour. Our results emphasize the importance of early-life social complexity for the development of social competence.
... However, of all group members it is usually the dominant female that performs the highest rates of territory defense and brood care (Desjardins et al., 2008b(Desjardins et al., , 2008c. Dominant group members usually maintain their social status and position for 3-12 months (Dierkes et al., 2005;Stiver et al., 2004), allowing for the behaviour of individuals of different status and sex to be reliably tracked for extended periods. Therefore, this group-living species offers a useful model for investigating relationships between AVP/OXT systems and social factors, some of which have already been examined in previous laboratory-based studies. ...
The neuropeptides arginine vasopressin (AVP) and oxytocin (OXT) are key regulators of social behaviour across vertebrates. However, much of our understanding of how these neuropeptide systems interact with social behaviour is centred around laboratory studies which fail to capture the social and physiological challenges of living in the wild. To evaluate relationships between these neuropeptide systems and social behaviour in the wild, we studied social groups of the cichlid fish Neolamprologus pulcher in Lake Tanganyika, Africa. We first used SCUBA to observe the behaviour of focal group members and then measured transcript abundance of key components of the AVP and OXT systems across different brain regions. While AVP is often associated with male-typical behaviours, we found that dominant females had higher expression of avp and its receptor (avpr1a2) in the preoptic area of the brain compared to either dominant males or subordinates of either sex. Dominant females also generally had the highest levels of leucyl-cystinyl aminopeptidase (lnpep)—which inactivates AVP and OXT—throughout the brain, potentially indicating greater overall activity (i.e., production, release, and turnover) of the AVP system in dominant females. Expression of OXT and its receptors did not differ across social ranks. However, dominant males that visited the brood chamber more often had lower preoptic expression of OXT receptor a (oxtra) suggesting a negative relationship between OXT signalling and parental care in males of this species. Overall, these results advance our understanding of the relationships between complex social behaviours and neuroendocrine systems under natural settings.
... For example, although most avian cooperative breeders were historically thought to form social groups primarily with closely related individuals (4), more recent work suggests that nearly half of all cooperatively breeding birds actually form groups comprising a high proportion of unrelated individuals (1). In contrast to societies with simpler group structure-those that typically comprise small, nuclear families with one breeding pair and one or more helpers that are offspring from previous broods (4)-these mixed-kin societies form via immigration of unrelated individuals of both sexes in addition to the retention of offspring born into the group (1,5). Moreover, immigrants often acquire breeding opportunities alongside natal individuals, resulting in plural breeding societies characterized by not only multiple breeding pairs, but also large groups and low but mixed kinship (6,7). ...
Although kin selection is assumed to underlie the evolution of sociality, many vertebrates-including nearly half of all cooperatively breeding birds-form groups that also include unrelated individuals. Theory predicts that despite reducing kin structure, immigration of unrelated individuals into groups can provide direct, group augmentation benefits, particularly when offspring recruitment is insufficient for group persistence. Using population dynamic modeling and analysis of long-term data, we provide clear empirical evidence of group augmentation benefits favoring the evolution and maintenance of complex societies with low kin structure and multiple reproductives. We show that in the superb starling (Lamprotornis superbus)-a plural cooperative breeder that forms large groups with multiple breeding pairs, and related and unrelated nonbreeders of both sexes-offspring recruitment alone cannot prevent group extinction, especially in smaller groups. Further, smaller groups, which stand to benefit more from immigration, exhibit lower reproductive skew for immigrants, suggesting that reproductive opportunities as joining incentives lead to plural breeding. Yet, despite a greater likelihood of becoming a breeder in smaller groups, immigrants are more likely to join larger groups where they experience increased survivorship and greater reproductive success as breeders. Moreover, immigrants form additional breeding pairs, increasing future offspring recruitment into the group and guarding against complete reproductive failure in the face of environmental instability and high nest predation. Thus, plural breeding likely evolves because the benefits of group augmentation by immigrants generate a positive feedback loop that maintains societies with low and mixed kinship, large group sizes, and multiple reproductives.
... Unlike other teleost fishes where offspring cannibalism is common (Manica, 2002;Pereira et al., 2017;Smith and Reay, 1991), N. pulcher rarely cannibalize their young and provide high quality care towards them (Heg and Hamilton, 2008;Jindal et al., 2017;von Siemens, 1990). Dominant females produce the majority of young within each group (Dierkes et al., 2005;Hellmann et al., 2015), and while all group members help care for young, dominant females usually provide the most care (Balshine et al., 2001;Desjardins et al., 2008;Heg and Hamilton, 2008;Taborsky and Grantner, 1998). These differences in reproduction and care provisioning likely contribute to the energetic costs incurred by dominants, which spend less time feeding (Sopinka et al., 2009) and maintain lower energy reserves than subordinates (Hellmann et al., 2016;Sopinka et al., 2009). ...
As many busy parents will attest, caring for young often comes at the expense of having time to feed and care for oneself. Galanin is a neuropeptide that regulates food intake and modulates parental care; however, the relative importance of galanin in the regulation of feeding versus caring by parents has never been evaluated before under naturalistic settings. Here, we assessed how expression of the galanin system varied in two brain regions, the hypothalamus (which regulates feeding) and the preoptic area (which modulates social behaviours including care) in a wild cichlid fish, Neolamprologus pulcher. Females with young had higher hypothalamic expression of galanin receptor 1a, and the highest expression of galanin and galanin receptor 1a was observed in females that foraged the least. However, expression of five other feeding-related neuropeptides did not change while females were caring for young suggesting that changes in the hypothalamic galanin system may not have been directly related to changes in food intake. The preoptic galanin system was unaffected by the presence of young, but preoptic galanin expression was higher in dominant females (which are aggressive, regularly reproduce and care for young) compared to subordinate females (which are submissive, rarely reproduce but often help care for young). Additionally, preoptic galanin expression was higher in fish that performed more territory defense. Overall, our results indicate that galanin has brain-region-specific roles in modulating both parental care and social status in wild animals.
... Finally, cooperation also regularly occurs among non-kin individuals in many species (Clutton-Brock 2002;Riehl 2011;Wilkinson et al. 2016;Teunissen et al. 2021), which does not support the prediction of kin-directed help. Such mixed-kin groups can arise (i) when individuals disperse and join a non-natal group, (ii) as the result of promiscuity and communal breeding, or (iii) after the death of one or both of the parents (Dierkes et al. 2005;Riehl 2013). ...
In cooperatively breeding species, group members may derive multiple benefits from helping to raise other individuals’ offspring, yet not all individuals do so. In this study, we tested predictions from the “kin selection”, “pay-to-stay”, “group augmentation” and “skills” hypotheses, to explain why group members feed nestlings of breeding placid greenbuls (Phyllastrephus placidus). In our study population, about 70% of the breeding pairs were accompanied by subordinates, and in 60% of these cases at least one subordinate helped in provisioning nestlings. In total, 80% of the subordinates were related to one or both breeders. In accordance with the “kin selection” hypothesis, and contrary to the “pay-to-stay” hypothesis, all the helpers were first-order kin of the breeding female (although relatedness to the breeding male did not explain variation in helping) and the presence of helpers was associated with increased survival of the breeding pair. However, the propensity to help varied among group members, as 46% of group members related to the breeding female did not feed nestlings. Younger helpers fed offspring more often than older ones, supporting the “skills” and “group augmentation” hypotheses. However, support for the “group augmentation” hypothesis was mixed since subordinate sex and group size did not explain additional variation in helping propensity and effort. We argue that in addition to indirect and direct benefits, also the costs of helping as well as other types of helping aside from provisioning must be considered to better understand variation in helping behavior.
... While the mechanisms of kinship dynamics presented here may not apply to non-pluralistic breeders, age-related changes in relatedness have been found in several cooperatively breeding vertebrates. In African wild dogs (Lycaon pictus), dwarf mongooses (Helogale parvula) and Lake Tanganyika cichlids (Neolamprologus pulcher) the relatedness of helpers to the dominant breeders is higher in younger than in older helpers [81][82][83] . These patterns are driven by turn-over of the dominant individuals in the philopatric sex and dispersal by groups, rather than by individuals, in the dispersing sex 82 . ...
The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness—the average relatedness of an individual to their social environment—therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual’s lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.
... The Lake Tanganyika princess (Neolamprologus pulcher) is a cooperatively breeding cichlid with low relatedness within groups and size-dependent reproductive queueing [31][32][33] (copyright: Dario Josi). (c) The Seychelles warbler (Acrocephalus sechellensis) has low withingroup relatedness and age-independent reproductive queueing 34-36 (copyright: Charli Davies). ...
Cooperatively breeding animals live longer than their solitary counterparts. The traditional explanation for this is that cooperative breeding evolves more readily in long-lived species. Here, we reverse this argument and show that long lifespans are an evolutionary consequence of cooperative breeding. Natural selection favours a delayed onset of senescence in cooperative breeders, relative to solitary breeders, because cooperative breeders have a delayed age of first reproduction due to reproductive queueing. Especially long lifespans evolve in cooperative breeders with age-dependent reproductive queueing. Finally, we show that lower genetic relatedness among group members leads to the evolution of longer lifespans. This is because selection against higher mortality is weaker when mortality reduces competition between relatives. Our results link the evolutionary theory of ageing with kin selection theory, demonstrating that the evolution of ageing in cooperative breeders is driven by the timing of reproduction and kin structure within breeding territories.
... This indicates that group switching probably accounts for many of our "extra-group" parentage cases, because extra-group reproduction would not be expected to correlate with offspring size (i.e., our proxy for "time since hatching"; see below for our discussion on accounting for historical conditions that might have been more conducive to cuckoldry). Other group-living cichlids, such as Julidochromis ornatus (Awata et al., 2005) and Neolamprologus pulcher (Dierkes et al., 2005), display similar decreasing relationships between the size/ age of offspring and their relatedness to same-group dominants, which can in part be attributable to the movement of adults among groups, and the replacement of breeders within groups. In N. multifasciatus, the movement of adults between groups could be stimu- (Hellmann et al., 2015). ...
Group‐living animals are often faced with complex reproductive decisions, namely how to partition within‐group reproduction, how to obtain extra‐group reproduction, and how these two means of reproduction should be balanced. The solutions to these questions can be difficult to predict because ecological conditions can affect the scopes for within‐group and extra‐group reproduction in complex ways. For example, individuals that are restricted from moving freely around their habitats may have limited extra‐group reproductive opportunities, but at the same time, groups may live in close proximities to one another, which could potentially have the opposite effect. The group‐living cichlid fish, Neolamprologus multifasciatus, experiences such ecological conditions, and we conducted an intensive genetic parentage analysis to investigate how reproduction is distributed within and among groups for both males and females. We found that cohabiting males live in ‘high‐skew’ societies, where dominant males monopolize the majority of within‐group reproduction, while females live in ‘low‐skew’ societies, where multiple females can produce offspring concurrently. Despite extremely short distances separating groups, we inferred only very low levels of extra‐group reproduction suggesting that subordinate males have very limited reproductive opportunities. A strength of our parentage analysis lies in its inclusion of individuals that spanned a wide age range, from young fry to adults. We outline the logistical circumstances when very young offspring may not always be accessible to parentage researchers, and present strategies to overcome the challenges of inferring mating patterns from a wide age range of offspring.
... These fish live in groups consisting of a dominant male-female breeding pair and 1-20 mixed sex subordinates (Balshine et al., 2001;Heg et al., 2004a). In the wild, group membership is relatively stable and dominant group members typically maintain these positions for many months (Dierkes et al., 2005;Stiver et al., 2004). Dominant males are often polygynous and spend much of their time shuttling between the different territories that they hold (Desjardins et al., 2008a;Wong et al., 2012), while dominant females remain on one territory and generally perform the highest rates of territory defense and brood care of any group member (Desjardins et al., 2008b,c). ...
Individuals that live in groups experience different challenges based on their social rank and sex. Glucocorticoids have a well-established role in coordinating responses to challenges and glucocorticoid levels often vary between ranks and sexes. However, the neuroendocrine mechanisms regulating glucocorticoid dynamics in wild groups are poorly understood, making it difficult to determine the functional consequences of differences in glucocorticoid levels. Therefore, we observed wild social groups of a cooperatively breeding fish (Neolamprologus pulcher) and evaluated how scale cortisol content (an emerging method to evaluate cortisol dynamics in fishes) and expression of glucocorticoid-related genes varied across group members. Scale cortisol was detectable in ~50% of dominant males (7/17) and females (7/15)-but not in any subordinates (0/16)-suggesting that glucocorticoid levels were higher in dominants. However, the apparent behavioural and neuroendocrine factors regulating cortisol levels varied between dominant sexes. In dominant females, higher cortisol was associated with greater rates of territory defense and increased expression of corticotropin-releasing factor in the preoptic and hypothalamic regions of the brain, but these patterns were not observed in dominant males. Additionally, transcriptional differences in the liver suggest that dominant sexes may use different mechanisms to cope with elevated cortisol levels. While dominant females appeared to reduce the relative sensitivity of their liver to cortisol (fewer corticosteroid receptor transcripts), dominant males appeared to increase hepatic cortisol breakdown (more catabolic enzyme transcripts). Overall, our results offer valuable insights on the mechanisms regulating rank-and sex-based glucocorticoid dynamics, as well as the potential functional outcomes of these differences.
... They live in stable groups with high reproductive skew and up to 25 helpers that engage in different forms of cooperative behaviour (Taborsky, 1984(Taborsky, , 1985Taborsky & Limberger, 1981). Helpers that vary in relatedness to the breeders can either stay in the territory and help or disperse and breed independently Dierkes et al., 2005;Heg et al., 2011;Hellmann et al., 2016;Taborsky & Limberger, 1981), and cooperative behaviour is used to appease the dominant breeders and prevent punishment and eviction Fischer et al., 2014;Naef & Taborsky, 2020;. Our study suggests that burrowing frequency in naked mole-rats decreased with age and body mass, which is consistent with recent research on age-related behavioural variation in naked mole-rats (Gilbert et al., 2020). ...
It has been proposed that naked mole-rat (Heterocephalus glaber) societies resemble those of eusocial insects by showing a division of labour among non-breeding individuals. Earlier studies suggested that non-breeders belong to distinct castes that specialise permanently or temporarily in specific cooperative tasks. In contrast, recent research on naked mole-rats has shown that behavioural phenotypes are continuously distributed across non-breeders and that mole-rats exhibit considerable behavioural plasticity suggesting that individuals may not specialise permanently in work tasks. However, it is currently unclear whether individuals specialise temporarily and whether there is a sex bias in cooperative behaviour among non-breeders. Here, we show that non-breeding individuals vary in overall cooperative investment, but do not specialise in specific work tasks. Within individuals, investment into specific cooperative tasks such as nest building, food carrying and burrowing is positively correlated, and there is no evidence that individuals show trade-offs between these cooperative behaviours. Non-breeding males and females do not differ in their investment in cooperative behaviours and show broadly similar age and body mass related differences in cooperative behaviours. Our results suggest that non-breeding naked mole-rats vary in their overall contribution to cooperative behaviours and that some of this variation may be explained by differences in age and body mass. Our data provide no evidence for temporary specialisation, as found among some eusocial insects and suggest that the behavioural organisation of naked mole-rats resembles that of other cooperatively breeding vertebrates more than that of eusocial insect species.
... (c) Finally, N. pulcher groups consist of a mixture of related and unrelated individuals. Relatedness to breeders declines with helper age, so that large adult helpers, which are most efficient in providing help, are usually unrelated to the breeder's offspring and beneficiaries of help (Dierkes et al., 2005). Opposite to cooperative systems driven by kin selection, but in accordance with the pay-to-stay mechanism, in N. ...
... These fish live in social groups consisting of a dominant female-male breeding pair and between 1-20 subordinate helpers (Balshine et al., 2001;Heg et al., 2005), and larger groups are generally more stable and resilient to disturbances (Anderson et al., 2020;Heg et al., 2005). Individuals occasionally move between groups (Bergmüller et al., 2005;Dierkes et al., 2005;Hellmann et al., 2016;Stiver et al., 2007;Stiver et al., 2006) and fish strongly prefer to join larger groups (Reddon et al., 2011;Salena and Balshine, 2020); likely because individuals in large groups tend to have a lower workload and reduced risk of predation (Balshine et al., 2001;Heg et al., 2004a;Jungwirth et al., 2015). However, N. pulcher groups are structured in a linear, size-based dominance hierarchy (Dey et al., 2013;Wong and Balshine, 2011) in which dominants restrict subordinate growth and reproduction via aggressive acts Heg et al., 2004b;Hellmann et al., 2015). ...
Many animals live in groups yet grouping tendencies and preferences for groups of different sizes vary considerably between individuals. This variation reflects, at least in part, differences in how individuals evaluate and perceive their physical surroundings and their social environment. While such differences are likely related to individual variation in cognition, there have been few studies that have directly investigated how cognitive abilities are linked to individual grouping decisions. Therefore, in this study we assessed whether performance on a foraging-based reversal learning task is related to grouping preferences (a group of three fish versus a single fish) in a group-living cichlid fish, Neolamprologus pulcher. While most fish preferred to associate with the group over a single fish, individuals that completed the reversal learning task the quickest were the least interested in the group under elevated predation risk. In addition, fish that quickly completed the reversal learning task also adjusted their grouping preferences the most when predation risk increased. This result suggests that the observed relationship between learning performance and grouping decisions may be linked to individual differences in behavioural flexibility. Overall, our results offer valuable insight into the potential factors that underlie inter-individual variation in grouping decisions.
... Helpers fulfill size-dependent tasks, with smaller helpers mainly invest in shelter maintenance and defense against egg predators, while larger helpers invest in defense against intruding conspecifics and fish predators (Figure 12.2) (Bruintjes & Taborsky, 2011;Groenewoud et al., 2016). The relatedness between helpers and breeders is low and decreases with increasing helper age, while it is higher among helpers of similar age (Dierkes, Heg, Taborsky, Skubic, & Achmann, 2005;Hellmann et al., 2016). Helpers that are related to the dominant female show a lower amount of help during egg care than unrelated ones (Zöttl et al., 2013). ...
Cooperative interactions are widespread in the animal kingdom. Their occurrence can be explained by mutually non-exclusive benefits increasing an individual's (1) indirect fitness by cooperating with kin, and (2) direct fitness by mutually or reciprocally cooperating with others. Many cooperative behaviors require well-developed neuroendocrine mechanisms regulating their quantity and quality. Fishes offer great opportunities to increase our insight into ultimate and proximate questions of cooperation. Their social systems range from solitary- and pair-living to lose fission–fusion groups and highly complex societies. Cooperative interactions are an essential part of the behavioural repertoire of most fish species, occurring in a variety of social situations like predator inspection, foraging, mating, or brood care. Such interactions take place among related and unrelated individuals and even between members of different species. This fascinating diversity allows investigating all crucial factors mediating cooperation, e.g., by studying behavioural interactions within and between species, by applying comparative approaches between taxonomic groups and by using state-of-the-art genetic and neuroendocrine technologies to resolve the underlying mechanisms. This chapter provides an overview of the mechanisms and functions of cooperative behaviour in fishes, with the overall aim to illuminate the evolution of cooperative behaviour in general.
... It is likely that the high frequency of extra-paternity promotes strong aggressive competition among juveniles in this species. Although several previous studies have examined the sex-dependent dispersal (Clarke et al. 1997;van Dongen et al. 2014) and territorial inheritance (Dierkes et al. 2005;Stiver et al. 2006) of cichlids, we were unable to determine the sexes of focal juveniles, owing to the difficulty of sexing in the field (Tanaka et al. 2015) and, accordingly, future studies should focus on whether the sex of juveniles affects sibling aggression in this species. ...
Siblings often compete for limited resources, such as food provided by their parents. However, although several functions of nonlethal sibling (nonsiblicidal) aggression have been proposed, there is currently little empirical evidence for these, apart from food monop-olization. Here, we investigated the functions of nonlethal sibling aggression in the biparental-caring territorial herbivorous cichlid Varibilichromis moorii. We found that the juveniles of this species are highly aggressive and that larger juveniles are more aggressive toward their smaller siblings. Larger juveniles feed on algae more frequently than smaller siblings, thereby indicating a dominance hierarchy. Sibling aggression decreased when algae in the nest was experimentally removed. Furthermore, the removal of smaller juveniles decreased sibling aggression among the remaining larger juveniles, whereas the removal of larger juveniles increased aggression among smaller juveniles. The algal feeding rate of juveniles only increased when larger individuals were removed from the nest. Moreover, larger juveniles attained higher growth rates and remained in natal nests longer than smaller individuals. Our results indicate that sibling aggression may facilitate the monopolization of resources by larger juveniles and extend the parental care period. Interestingly, a small subset of juveniles was observed to migrate to other nests. These juveniles were larger than those of the host brood, and their growth rate increased within the new nests. We suggest that subordinate juveniles may disperse from natal nests and sneak into new nests to enhance their rank, which may represent a novel example of a "best of a bad job" strategy associated with sibling competition.
... Griffin and West 2003;Green et al. 2016), in many instances, cooperation also occurs among non-kin individuals (Clutton-Brock 2002;Riehl 2013). Such non-kin cooperative groups may arise (i) when individuals disperse and join a non-natal group, (ii) as the result of promiscuity and communal breeding, or (iii) after the death of one or both of the parents (Dierkes et al. 2005;Riehl 2013). ...
... These fish also have a clear linear size-based dominance hierarchy, with increasing body size associated with increasing rank (Balshine-Earn et al., 1998). Natural groups regularly experience turnover of group members as helpers join or leave a group, or when group members perish Stiver et al., 2004;Wong and Balshine, 2011b), with breeders estimated to be replaced a median of every 198-274 days (Dierkes et al., 2005). Thus, this system provides a convenient evolutionary context to evaluate the impacts of group size on behavioral and metabolic responses to social instability and recoverability. ...
Intra-group social stability is important for the long-term productivity and health of social organisms. We evaluated the effect of group size on group stability in the face of repeated social perturbations using a cooperatively breeding fish, Neolamprologus pulcher In a laboratory study, we compared both the social and physiological responses of individuals from small versus large groups to the repeated removal and replacement of the most dominant group member (the breeder male), either with a new male (treatment condition) or with the same male (control condition). Individuals living in large groups were overall more resistant to instability but were seemingly slower to recover from perturbation. Members of small groups were more vulnerable to instability but recovered faster. Breeder females in smaller groups also showed greater physiological preparedness for instability following social perturbations. In sum, we discover both behavioral and physiological evidence that living in larger groups helps to dampen the impacts of social instability in this system.
... Harems are socially and genetically structured, with higher relatedness within subgroups compared to members of different subgroups within the same harem (Josi et al., 2019). As in other cooperatively breeding cichlids, relatedness between breeders and helpers declines strongly with increasing helper size (Dierkes, Heg, Taborsky, Skubic, & Achmann, 2005). Group members usually stay close to protective shelters, which they typically dig out themselves Heg, Bachar, & Taborsky, 2005). ...
In cooperatively breeding societies dominant breeders are assisted by other individuals in raising their young. In many of these species helping behaviours and their benefits for breeders have been studied by investigating the helpers' contribution to direct offspring care, even though a significant proportion of help is not targeted specifically to offspring. Here, we investigated how breeders and helpers share the effort in shelter maintenance and how their investment is influenced by the presence of dependent young in the cooperatively breeding cichlid Neolamprologus savoryi. Shelters provide essential protection from predators, independently of a group's breeding status. Shelter maintenance is costly in terms of time investment and energy expenditure. In the field we manipulated the workload of groups that differed in the presence and number of helpers and the reproductive state of breeders by increasing the need for digging out the breeding shelter. Helper presence correlated with workload reduction of dominant females, even in the absence of dependent young. This emphasizes the importance of shelters for the whole group, independently of the current reproductive status of the breeding pair. The described benefits increased with the number and body size of the helpers. Additionally, breeding females and helpers visited the breeding chamber more often if young were present, and helper presence enhanced the reproductive success of breeders. These findings highlight the importance of studying the role of helpers and their benefits to breeders not only in the context of direct brood care, but also for other cooperative tasks, in order to understand the evolution of complex animal societies
... However, a growing number of studies have found low mean levels of genetic relatedness within animal social groups, especially in tropical birds (Cockburn, 1998;Riehl, 2013), with the presence of both related and unrelated group members (e.g. dwarf mongoose, Helogale parvula: Creel & Rabenold, 1994; daffodil cichlid, Neolamprologus pulcher: Dierkes, Heg, Taborsky, Skubic, & Achmann, 2005; grey-throated babbler, Stachyris nigriceps: Kaiser, Martin, Oteyza, Armstad, & Fleischer, 2018). With no indirect benefits, why should unrelated individuals help and how much should they help? ...
In cooperatively breeding animals, genetic relatedness among group members often determines the extent of reproductive sharing, cooperation and competition within a group. Studies of species for which cooperative behaviour is not entirely based on kinship are key for understanding the benefits favouring the evolution and maintenance of cooperative breeding among nonrelatives. In the cooperatively breeding chestnut-crested yuhina, Yuhina everetti, a songbird endemic to Borneo, we tested whether unrelated helpers are more likely to gain parentage than are related helpers consistent with the hypothesis that inbreeding risk constrains reproduction by related helpers. We also examined whether related or unrelated helpers provision broods more because of differences in their potential indirect or direct fitness benefits of helping. Kin structure of breeding groups (breeding pair and up to eight helpers of both sexes, median = 2 helpers, 96% of 57 pairs had helpers) based on genetic analysis was mixed; 48% of 76 breeder/helper dyads were first-order (26%) or second-order (22%) relatives of one or both members of the breeding pair, and 52% were nonrelatives. Only unrelated male and female helpers gained parentage, and helpers did not differ in their provisioning rate according to their relatedness to the broods. We documented quasi-parasitism or co-breeding by female helpers in 14% of 29 broods and extrapair paternity by male helpers in 21% of 47 broods. This rate of extrapair paternity is relatively high among the few tropical species examined but fit with predictions for mixed-kin groups where inbreeding is avoided. These findings support the emerging pattern for cooperative breeding in birds with mixed-kin groups, wherein unrelated helpers are more likely to gain parentage than are related helpers and helping effort is not necessarily predicted by kinship.
... Neolamprologus pulcher is a cichlid species endemic to Lake Tanganyika, Zambia. It lives in social groups composed of a dominant breeding pair and 1e25 subordinate helpers, which may or may not be related to the breeding pair (Balshine-Earn, Neat, Reid, & Taborsky, 1998;Dierkes, Heg, Taborsky, Skubic, & Achmann, 2005;Taborsky & Limberger, 1981). The helpers contribute to territory maintenance, defence and tending the dominants' brood. ...
Social learning about predation threat during early ontogeny can be beneficial in developing appropriate antipredator behaviours. While such learning can be achieved through direct interactions between offspring and parents, it is unknown whether young animals can also learn appropriate responses towards different heterospecifics posing different levels of threat through inadvertent information obtained from witnessing parental interactions with these heterospecifics. In this study, we split sibling groups of the cooperatively breeding cichlid Neolamprologus pulcher and raised them with or without parents. Both rearing groups repeatedly received visual and olfactory cues from four types of fish (predators, egg predators, herbivores and conspecifics) during a 4-week experience phase. After a ‘neutral phase’ of 4 months under identical conditions and without further fish stimuli, individuals from both rearing conditions were tested for their response towards the same four stimulus species. Unlike those reared with parents, the fish reared without parents spent significantly more time in safety and were more vigilant towards the predator, whereas responses to the other three species did not differ. As during the experience phase parental responses towards the stimulus fish were unexpectedly low and indiscriminate, our results suggest that young N. pulcher reverse their innate fear of predators when observing parents being unresponsive to a threat (‘observational conditioning’). We suggest that learned reduction of fear can be a potent mechanism to prevent responding to false alarms and mitigate potentially harmful effects of chronically elevated predation stress.
... East of this colony, stones are largely absent and no N. pulcher can be found for several hundred meters. We are confident that fish we could not recapture near the original tagging location had died rather than dispersed outside of our working range, because (i) the population of Kasakalawe Point clusters into distinct colonies interspersed by long stretches of uninhabited terrain (Heg et al. 2008;Hellmann et al. 2016), and (ii) dispersal typically occurs within rather than between colonies (Stiver et al. 2004;Dierkes et al. 2005;Stiver et al. 2007;Heg et al. 2008). The focal colony of the current study covered an area of roughly 30 × 30 m (Jungwirth et al. 2015a), and was comprised of between 135 and 157 groups in a given year, several of which persisted throughout the whole observation period between September 2011 and November 2013 (Jungwirth and Taborsky 2015). ...
Tracking wild animals over long periods of time is a non-trivial challenge. This has caused a bias in the availability of individual-based long-term datasets with the majority including birds and mammals. Visual Implant Elastomer (VIE) tags are now a widely used technique that may facilitate the collection of such data for fish and amphibians. However, VIE tags might have important drawbacks. Overall, four potential issues with VIE tags have been proposed: tag loss or misidentification, limited number of individual identifiers, enhanced mortality risk, and effects on intra-specific interactions. Here, we present three experiments in which we investigated these potential problems with VIE tagging in small freshwater fish both in the laboratory and in the wild, using the cooperatively breeding Lake Tanganyika cichlid Neolamprologus pulcher. We find VIE tags to be generally suitable for work with these fish as they did not impair survival, were recognisable up to 2 years after injection, and did not generally disturb group formation. Nevertheless, we identify specific issues of VIE tagging, including colour- and position-dependent variation in tag identification rates, and indications that specific colours may influence social behaviour. Our results demonstrate the suitability of VIE tags for long-term studies on small freshwater fish, while also highlighting the need of validating this method carefully for any species and study.
Significance statement
Information on the survival, dispersal, and reproductive success of wild individuals across their lifespan is among the most valuable data in Behavioural Ecology. Because tracking of free-ranging individuals over extended periods of time is challenging, there exists a bias in the taxonomic distribution of such long-term datasets. Here, we investigate the suitability of visible implant elastomers (VIE) as a tracking technique to allow for the collection of such data also in small tropical freshwater fish. We show that VIE tags neither alter social behaviour in our study species, nor do they reduce survival, but they enable the tracking of wild individuals across years. We also identify colours and tag positions that are less suitable. We conclude that VIE tags can help produce long-term datasets also for small fish, provided certain precautions are met.
The age of individuals has consequences not only for their fitness and behaviour but also for the functioning of the groups they form. Because social behaviour often changes with age, population age structure is expected to shape the social organization, the social environments individuals experience and the operation of social processes within populations. Although research has explored changes in individual social behaviour with age, particularly in controlled settings, there is limited understanding of how age structure governs sociality in wild populations. Here, we synthesize previous research into age-related effects on social processes in natural populations, and discuss the links between age structure, sociality and ecology, specifically focusing on how population age structure might influence social structure and functioning. We highlight the potential for using empirical data from natural populations in combination with social network approaches to uncover pathways linking individual social ageing, population age structure and societal functioning. We discuss the broader implications of these insights for understanding the social impacts of anthropogenic effects on animal population demography and for building a deeper understanding of societal ageing in general.
This article is part of the discussion meeting issue ‘Understanding age and society using natural populations’.
The age of individuals has consequences not only for their fitness and behaviour, but also for the functioning of the groups they form. Because social behaviour often changes with age, population age structure is expected to shape the social organisation, the social environments individuals experience, and the operation of social processes within populations. Although research has explored changes in individual social behaviour with age, particularly in controlled settings, there is limited understanding of how age structure governs sociality in wild populations. Here, we synthesise previous research into age-related effects on social processes in natural populations, and discuss the links between age structure, sociality and ecology, specifically focusing on how population age structure might influence social structure and functioning. We highlight the potential for using empirical data from natural populations in combination with social network approaches to uncover pathways linking individual social ageing, population age structure and societal functioning. We discuss the broader implications of these insights for understanding the social impacts of anthropogenic effects on animal population demography, and for building a deeper understanding of societal ageing in general.
In some species, permanent curtailment of reproduction part‐way through the lifespan of adult females is a feature of their evolved life history. The existence of such a post‐reproductive life stage is apparently rare; reasonably robust evidence for this is confined to only six species (humans, Asian elephants and four whales). That it occurs at all appears to contradict our view of natural selection operating to maximize fitness and special circumstances must exist to explain its occurrence. We evaluate the main hypotheses posited to explain the evolution of this life stage, why it occurs in a restricted group of animals, and why only in females. We bring together literature from multiple biological disciplines and levels of enquiry, ranging through evolutionary ecology, developmental biology, physiology, neuroscience, molecular biology, and human medicine. We conclude that while time‐limited fertility is not in itself adaptive, the duration of subsequent survival is likely to be linked to inclusive fitness benefits. We present a new hypothesis which posits that the duration of female fertility in certain long‐lived, highly encephalised species, with no post‐natal oogenesis, is limited by the need for intense screening of oocyte mitochondria. This is required to support endothermy coupled with the very high energy requirement for the development and maintenance of the exceptionally large brain size required for complex social living. This limits the number and shelf‐life of oocytes, creating an antagonistically pleotropic effect that is beneficial to the production of high performing offspring but carries the later life cost of time‐limited female fertility. But the end of the fertile period is no time to die. Inclusive fitness benefits arising from protracted parental care of offspring, overlapping generations, and kin group structures means that continued survival of post‐reproductive females is favoured by selection. We suggest further lines of research to test these ideas.
In cooperatively breeding species, subordinates can obtain group membership through social interactions with other group members or by providing services such as helping with territory defence. Large subordinate individuals, which can reproduce, are expected to adjust their behaviour as a function of the demand of help and group size because if the environmental conditions allow, they may either leave the group to start breeding or queue for the breeding position in their natal group. The number of helpers in a group is expected to affect the need of help by dominants and consequently also the level of subordination shown by helpers. In a series of field experiments, we manipulated the need of help and the opportunities for subordinates to show submissive behaviour in a wild population of the cooperatively breeding species Neolamprologus pulcher. We assessed if group size determines the social behavioural strategy of large subordinate individuals. When experimentally eliciting submissive behaviour, large subordinates from small groups showed a lower frequency of submissive behaviour compared to large groups; moreover, they tended to show a higher frequency of sand digging than in large groups. In contrast, neither territory defence in the presence of a heterospecific egg and larvae predator nor dispersal propensity, measured as prospecting frequency in neighbouring territories, was affected by group size. A principal component analysis revealed that prospecting is uncorrelated with submissive behaviour and helping behaviour. Our results suggest that group size may be involved in shaping behavioural phenotypes of juvenile subordinates.
Social evolution is tightly linked to dispersal decisions, but the ecological and social factors selecting for philopatry or dispersal often remain obscure. Elucidating selection mechanisms underlying alternative life histories requires measurement of fitness effects in the wild. We report on a long-term field study of 496 individually marked cooperatively breeding fish, showing that philopatry is beneficial as it increases breeding tenure and lifetime reproductive success in both sexes. Dispersers predominantly join established groups and end up in smaller groups when they ascend to dominance. Life history trajectories are sex specific, with males growing faster, dying earlier, and dispersing more, whereas females more likely inherit a breeding position. Increased male dispersal does not seem to reflect an adaptive preference but rather sex-specific differences in intrasexual competition. Cooperative groups may thus be maintained because of inherent benefits of philopatry, of which females seem to get the greater share in social cichlids.
Members of social groups may negotiate among each other about the exchange of goods and services. If this involves asymmetries between interacting partners, for instance in condition, power, or expected payoffs, coercion may be involved in the bargain. Cooperative breeders are excellent models to study such interactions, because asymmetries are inherent in the relationship between dominant breeders and subordinate helpers. Currently it is unclear whether punishment is used to enforce costly cooperation in such systems. Here we investigated experimentally in the cooperatively breeding cichlid Neolamprologus pulcher whether alloparental brood care provided by subordinates is contingent on enforcement by dominant breeders. We manipulated first the brood care behavior of a subordinate group member and then the possibility of the dominant breeders to punish idle helpers. When subordinates were prevented from providing brood care, breeders increased their attacks on them, which triggered increased alloparental brood care by helpers as soon as this was again possible. In contrast, when the possibility to punish helpers was prevented, energetically costly alloparental brood care did not increase. Our results confirm predictions of the pay-to-stay mechanism causing alloparental care in this species and they suggest more generally that coercion can play an important role in the control of cooperation.
Cooperatively breeding animals live longer than their solitary counterparts. This has been suggested for birds, mole rats, and social insects. A common explanation for these long lifespans is that cooperative breeding evolves more readily in long‐lived species because lower mortality reduces the rate of territory turnover and thus leads to a limitation of breeding territories. Here, we reverse this argument and show that—rather than being a cause for its evolution—long lifespans are an evolutionary consequence of cooperative breeding. In evolutionary individual‐based simulations, we show that natural selection favors a delayed onset of senescence in cooperative breeders, relative to solitary breeders, because cooperative breeders have a delayed age of first reproduction as helpers wait in a reproductive queue to obtain breeder status. Especially long lifespans evolve in cooperative breeders in which queue positions depend on the helpers’ age rank among the helpers within the breeding territory. Furthermore, we show that lower genetic relatedness among group members leads to the evolution of longer lifespans. This is because selection against higher mortality is weaker when mortality reduces competition for breeding between relatives. Our results link the evolutionary theory of ageing with kin selection theory, demonstrating that the evolution of ageing in cooperative breeders is driven by the timing of reproduction and kin structure within breeding territories.
Cooperative breeders are species in which individuals beyond a pair assist in the production of young in a single brood or litter. Although relatively rare, cooperative breeding is widespread taxonomically and continues to pose challenges to our understanding of the evolution of cooperation and altruistic behavior. Bringing together long-term studies of cooperatively breeding birds, mammals, and fishes, this volume provides a synthesis of current studies in the field. The chapters are organised by individual studies of particular species or (in the case of mole-rats) two closely related cooperatively breeding species. Each focuses not only on describing behavior and ecology but also on testing evolutionary hypotheses for the form and function of the diverse and extraordinary cooperative breeding lifestyles that have been discovered. This unique and comprehensive text will be of interest to graduate students and researchers of behavioral ecology and the evolution of cooperation.
Cooperative breeders are species in which individuals beyond a pair assist in the production of young in a single brood or litter. Although relatively rare, cooperative breeding is widespread taxonomically and continues to pose challenges to our understanding of the evolution of cooperation and altruistic behavior. Bringing together long-term studies of cooperatively breeding birds, mammals, and fishes, this volume provides a synthesis of current studies in the field. The chapters are organised by individual studies of particular species or (in the case of mole-rats) two closely related cooperatively breeding species. Each focuses not only on describing behavior and ecology but also on testing evolutionary hypotheses for the form and function of the diverse and extraordinary cooperative breeding lifestyles that have been discovered. This unique and comprehensive text will be of interest to graduate students and researchers of behavioral ecology and the evolution of cooperation.
Cooperative breeders are species in which individuals beyond a pair assist in the production of young in a single brood or litter. Although relatively rare, cooperative breeding is widespread taxonomically and continues to pose challenges to our understanding of the evolution of cooperation and altruistic behavior. Bringing together long-term studies of cooperatively breeding birds, mammals, and fishes, this volume provides a synthesis of current studies in the field. The chapters are organised by individual studies of particular species or (in the case of mole-rats) two closely related cooperatively breeding species. Each focuses not only on describing behavior and ecology but also on testing evolutionary hypotheses for the form and function of the diverse and extraordinary cooperative breeding lifestyles that have been discovered. This unique and comprehensive text will be of interest to graduate students and researchers of behavioral ecology and the evolution of cooperation.
Cichlid fishes are champion caregivers that protect, clean, aerate, and sometimes even feed their young. This tropical fish family’s extensive species radiation combined with great diversity in care habits make cichlids immensely useful models for studying the evolution of parental care. In this chapter, we review the diverse ways that care is provided (~1/3 of species guard young on the ground and 2/3 mouthbrood) and the variation in sex of the caregiver (42% of species have biparental care, 58% show the derived state of female-only care). Substrate guarding, the ancestral form of care, is especially common among New World cichlids. In contrast, mouthbrooding, dominates in African clades. We also describe two forms of expanded (allo) care: (1) brood mixing where parents care for non-descendant young; and (2) cooperative breeding with joint care by an entire social group. Such cooperative breeding, arguably one of the most socially complex breeding systems, has arisen at least 5X among cichlids, all within a single clade, the Lamprologines of Lake Tanganyika. Using one well-studied cooperative species, Neolamprologus pulcher, as an example, we review the various possible explanations for the evolution of cooperative care. We conclude by discussing some exciting future directions for the study of parental care in cichlids.
The complex social behaviour of cichlids has fascinated scientists and hobbyists alike for almost 100 years. In this chapter, we review the breadth and complexity of cichlid behaviour, particularly with respect to social interactions. We present the case that cichlids are one of the best model systems for understanding both the mechanisms and evolution of behaviour. This is due to the fact that cichlids can be observed without being greatly disturbed, both in the aquarium and field and because of the unique opportunity to experimentally manipulate their environment and behaviour. We first give a brief account of the diversity of social systems in the cichlids and the diverse research in this area, from the very early work of authors like Curtis, Noble, and Baerends, to modern studies into the dynamics and structure of social behaviour in these fish. In Sect. 2, we explore the causal factors leading to the evolution of social complexity, discussing the occurrence and evolution of different social systems across ecological and life-history contexts. We investigate the behavioural complexity displayed by cichlids in Sect. 3, including a brief treatment of the different modalities of behavioural interactions. In Sect. 4, we discuss the immense potential for using cichlids as model species in studying social and behavioural evolution, before ending in Sect. 5 with exciting future directions for research employing the latest technical advances in both the laboratory and field.
Helping behaviour in some cooperative breeders is apparently maintained by a combination of coercion and reciprocity. In such pay-to-stay systems, alloparental brood care of subordinate group members functions as a service to dominants, which tolerate subordinates based on how much help they provide. Cooperative territory defence is a key task of cooperative breeders, but it is unknown how territory defence by subordinates is socially regulated. Diverse costs and benefits associated with defending the territory against different threats suggest that these defence behaviours may be maintained through divergent selection regimes, and they might be regulated through different social processes. In the cooperatively breeding cichlid fish Neolamprologus pulcher, unrelated subordinates help defend the territory against egg predators even if they do not participate in reproduction and therefore do not suffer direct or indirect fitness costs through predators of eggs. This behaviour has therefore been interpreted as altruistic service to dominants. Subordinates also defend the group territory against predators of juveniles and adults, which might at least partly reflect their own direct fitness interests and could be maintained through mutualistic interactions among group members. Here, we directly compared the regulation of these two types of defence behaviours and tested whether they are enforced by breeders. We prevented subordinates from defending the territory against egg predators or predators of adults and observed whether they received more aggression in response to this treatment. We found that subordinates received more aggression from breeders after withholding defence against egg predators, but not after withholding defence against fish predators. This suggests that territory defence against egg predators by helpers is enforced by breeders and hence subject to negotiations and trading, whereas defence against fish predators is probably based on mutualistic fitness benefits.
Altruism is of great interest to evolutionary psychologists because of the apparent dilemma it presents to Darwin’s theory of natural selection, a dilemma he acknowledged
“if it could be proved that any part of the structure of any one species had been formed for the exclusive good of another species, it would annihilate my theory, for such could not have been produced through natural selection” (Darwin, 1859, 189).
To overcome this dilemma evolutionary psychologists have engaged in the pursuit of explanations for apparent acts of altruism. From this pursuit a number of possible explanations have been suggested. Two of the most widely accepted explanations are kin selection (Hamilton, 1964) and reciprocal altruism (Trivers 1971). However many other explanations have been proposed from induced altruism (Trivers, 1985), to costly signaling theory (Waynforth, 2011; Zahavi & Zahavi, 1997) to more complex multi-level and group selection models (Boyd & Richerson, 1982; Feldman & Cavalli-Sforna, 1976).
Large male helpers in the cooperatively breeding cichlid Neolamprologus pulcher gain reproductive success by parasitizing the reproductive effort of male territory owners. Under controlled, experimental conditions we examined the genetic relatedness between the members of brood pairs (n 5 14), their male helpers (n 5 8), and offspring (n 5 292) in seven families. We used multilocus DNA fingerprinting to check for potential reproductive parasitism by male helpers and to assess their fertilization success. Of offspring produced in these families, 10.3% were sired by helpers. In parasitized broods, helper fertilization success varied between 12.5% and 35.8%. Male helpers parasitized parental reproduction when their body size exceeded 4.5 cm standard length (SL), even though sexual maturity may be reached much earlier (3.5 cm SL). Two of three parasitic helpers were punished by severe aggressive attacks when parasitizing the reproduction of breeders, which led to their expulsion from the territory. This study demonstrates a potential fitness benefit to broodcare helpers that is often neglected. It also points to the delicate balance that may exist between cooperative and competitive behavior in cooperatively breeding species. Key words: Lake Tanganyika, cichlids, cooperative breeding, DNA fingerprinting, Neolamprologus pulcher, N. brichardi, reproductive competition. (Behav Ecol 10:510-515 (1999))
kingroup is an open source java program implementing a maximum likelihood approach to pedigree relationships reconstruction and kin group assignment. kingroup implements a new method (currently being performance tested) for reconstructing groups of kin that share a common relationship by estimating an overall likelihood for alternative partitions. A number of features found in kinship (Goodnight & Queller 1999) have also been implemented to make them available outside the Classic Macintosh OS platform for the first time.
We established pedigree relations in three wild common marmoset social groups for which observational data were available, together with genotypes of some individuals from neighboring groups. Relatedness of 40 individuals were based on 11 microsatellite loci amplified from nDNA obtained noninvasively from plucked hair. The wild marmosets were only half as variable as a captive population characterized previously: 2–6 alleles/locus; HO = 0.41 and HE = 0.35. Parentage exclusion probabilities were 61.8% for an offspring and one alleged parent and 90.7% for an offspring with one confirmed and one alleged parent. Each group (n = 5–14 individuals) had two breeding females and 2 adult males. Within each group the infants and reproductively inactive adults were closely related to at least the breeding females; the latter were related to each other as closely as mother/infant pairs or sisters. Relatedness of adult males was lower, indicating recent intergroup dispersal. Genetic data confirm Callithrix jacchus live in relatively stable extended family groups of closely related individuals. Matings occurred preferentially among the least related adults and most infants were fathered by the dominant male. The genetic data are consistent with polygynmonandry as are the field observations. Callithrix have variable mating systems, ranging from monogamy to polyandry to polygyny within social groups plus extragroup copulations; our data provide no evidence for polyandry and are inconclusive with respect to extragroup paternity. Nevertheless, noninvasive multilocus genotyping methods will resolve these questions when longer-term studies of entire populations are undertaken.
In cooperative breeders, mature males may compete for fertilizations. In this study, we measured the degree of multiple paternity
in a natural population of a cooperatively breeding fish. Neolamprologus pulcher (Perciformes: Cichlidae) is a highly social cichlid endemic to Lake Tanganyika. We used highly variable microsatellite loci
to survey 12 groups with an average number of 10.6 brood care helpers per group and a total of 43 offspring (mean 3.6 per
brood). In 11 of 12 groups, all young were assigned to the dominant female. The dominant male sired all offspring in three
groups, part of the offspring in four groups, and in five groups, he had no paternity at all. In total, 44.2% of young were
not fathered by the current male territory owner. Multiple paternity was found in 5 of 12 broods (41.7 %), with 8 of 35 young
(22.9 %) being sired by males other than the respective territory owners. This is an exceptionally high rate of extra-pair
paternity among cooperatively breeding vertebrates. Neither helpers present in these territories during collection nor neighbouring
males were unequivocally assigned to have sired these extra-pair young. However, behavioural observations suggest that male
helpers may have produced these young before being expelled from the territory in response to this reproductive parasitism.
We discuss these results in the light of reproductive skew theory, cooperative breeding in vertebrates and alternative reproductive
tactics in fish.
Neolamprologus pulcher, a cooperatively breeding cichlid fish from Lake Tanganyika, lives in permanent social groups comprising one breeding pair and helpers of both sexes. Variation in group size (1-14 helpers) provides an opportunity to investigate factors that affect how many helpers remain in a group and in turn how group size affects reproductive success. This field study showed that larger groups live in larger territories with more shelter. Group size was more strongly correlated with territory quality than with breeder size. Experimental enhancement of territory quality did not affect group size but group size decreased when territory quality was reduced. Breeders living in a large group benefit because such individuals feed more often and have lower workloads and greater reproductive success. Helpers in larger groups also fed more frequently but did not have lower workloads. This is one of the first experimental studies to examine the factors influencing group size in cooperative breeders.
Field data show that in the cichlid fish Lamprologus brichardi conspecifics other than the reproducing pair help in brood care and territory maintenance. The expected degree of relatedness between helpers and the eggs or larvae they tend lies between 0.25 and 0.5, decreasing with the helper's age. This decrease might influence the point of time at which helpers depart. Five other endemic Lake Tanganyika cichlids showing rather similar helping behaviour are described.
We measured the metabolic rates as a direct estimate of energy expenditure of individual Neolamprologus pulcher, a cooperatively breeding cichlid fish, when resting and when performing agonistic, submissive or digging behaviours in a
respirometer. Standard and routine metabolic rates increased linearly with body mass (range 0.9–8.4 g) when plotted on a doubly
logarithmic scale (linear regression equations: standard metabolic rate: log individual oxygen consumption rate = 0.65 + 0.86
log body mass; routine metabolic rate: log individual oxygen consumption rate = 0.75 + 0.86 log body mass). Routine metabolic
rates were, on average, 30% higher than standard metabolic rates. Submissive and agonistic behaviours raised routine metabolic
rates by factors of 3.3 and 3.9, respectively. Digging resulted in a 6.1-fold increase of routine metabolic rates. Differences
in metabolic rates between active and resting rates were statistically significant. However, those between the three behaviours
were not. Mean opercular beat frequencies correlated significantly with routine metabolic rates and with metabolic rates when
performing specific behaviours, which offers methodological prospects for field measurements. In N. pulcher, the high energy expenditure for submissive behaviour may indicate that this is a reliable signal. The considerable energy
expenditure involved in territory defence suggests that these costs should be considered in addition to risk in cost-benefit
analyses. This is the first study in which the energy expenditures of specific social and territory maintenance behaviours
of individual fish were measured directly by respirometry and within the usual social setting of the fish.
Measurement of reproductive skew in social groups is fundamental to understanding the evolution and maintenance of sociality, as it determines the immediate fitness benefits to helpers of staying and helping in a group. However, there is a lack of studies in natural populations that provide reliable measures of reproductive skew and the correlates of reproductive success, particularly in vertebrates. We present results of a study that uses a combination of field and genetic (microsatellite) data on a cooperatively breeding mongoose, the meerkat (Suricata suricatta). We sampled 458 individuals from 16 groups at two sites and analyzed parentage of pups in 110 litters with up to 12 microsatellites. We show that there is strong reproductive skew in favor of dominants, but that the extent of skew differs between the sexes and between different sites. Our data suggest that the reproductive skew arises from incest avoidance and reproductive suppression of the subordinates by the dominants. Copyright 2003.
Neolamprologus pulcher is a cooperatively breeding cichlid fish, in which helpers stay in their natal territory and help with brood care, territory defense, and maintenance. In this study we investigated helper effects by an experimental group size reduction in the field. After this manipulation, focal helpers in reduced groups tended to feed less, and small helpers visited the breeding shelter significantly more often than same-sized helpers in control groups. No evidence was found that remaining helpers compensated for the removed helpers by increasing territory defense and maintenance behavior. Breeders, however, did show a lower defense rate, possibly caused by an increase in brood care effort. Survival of fry was significantly lower in removal than control groups, which provides the first experimental proof in a natural population of fish that brood care helpers do effectively help. The data suggest that in small, generally younger, helpers, kin selection may be an important evolutionary cause of cooperation. Large helpers, however, who are generally older and less related to the breeders than small helpers are suggested to pay to be allowed to stay in the territory by helping. All group members benefit from group augmentation. Copyright 2005.
Canid social groups are typically thought to consist of extended families, that is, a dominant breeding pair and related nonbreeding subordinates, that principally obtain indirect fitness benefits from helping to raise the offspring of the dominant pair. Consequently, the monogamous pair has been viewed as the basic fundamental unit of canid social organization. However, there have been few genetic studies that have tested this assumption. We analyzed the parentage of red foxes (Vulpes vulpes) in a high-density (19.6--27.7 adult foxes/km-super-2) population in Bristol, UK, to determine (1) whether groups typically produced a single litter of cubs annually and (2) whether male and female foxes exhibited monogamous mating strategies. Social monogamy (the production of one litter in a social group) was observed or assumed in 54% of breeding attempts (N = 13 group-years). However, polyandrous and polygynous patterns of mating were common. Multiple paternity was confirmed in 38% of litters (N = 16) containing offspring with resolved maternity and paternity (N = 30 cubs); when including cubs with unresolved paternity (N = 20), multiple-paternity may have occurred in 69% of litters. Litters were sired by an average of 1.6 identified males (range = 1--4); when including cubs with unresolved paternity, litters may have been sired by up to seven males. Only 20% (6/30) of cubs with resolved maternity and paternity were sired by males within the social group. Within groups, dominant females did not breed with subordinate males; dominant males did breed with subordinate females. Dominant and subordinate females both produced cubs with dominant and subordinate males from other social groups. Mean adult relatedness in groups typically ranged from 0.15--0.35, indicative of second-order rather than first-order relatives. Copyright 2004.
Several hypotheses aim to explain the evolution of helping behavior, but conclusive experimental support for evaluating the relative importance of individual hypotheses is still lacking. We report on two field experiments conducted to test the “territory inheritance” and “pay-to-stay” hypotheses in the cooperatively breeding cichlid fish Neolamprologus pulcher The territory inheritance hypothesis was tested by removing one parent, which created breeding vacancies. In 39% of cases, same-sex helpers took over the breeding spot; in 44% of cases helpers continued helping new breeders, and 17% were evicted by new breeders. Helpers that were closely size matched to the removed breeder had a better chance of gaining the breeding spot Male helpers tended to continue helping after a takeover more often than females.The pay-to-stay hypothesis was tested-by temporarily removing helpers. Whereas breeders did not respond aggressively to removals, other group members attacked the removed helpers on their return, and 29% were eventually evicted. The returning helpers assisted more by increasing their rate of territory maintenance and defense and visiting the brood chamber more frequently Size and sex of removed helpers did not explain the observed aggressive reactions of other group members. Thus, our results support both hypotheses: N. pulcher needs to pay with help to be allowed to remain protected in the family group, and there they may inherit the natal territory. N. pulcher helpers gain direct benefits from helping behavior.
Note that an updated reference for Genepop is Rousset (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux (DOI: 10.1111/j.1471-8286.2007.01931.x)
The predictability of genetic structure from social structure and differential mating success was tested in wild baboons. Baboon populations are subdivided into cohesive social groups that include multiple adults of both sexes. As in many mammals, males are the dispersing sex. Social structure and behavior successfully predicted molecular genetic measures of relatedness and variance in reproductive success. In the first quantitative test of the priority-of-access model among wild primates, the reproductive priority of dominant males was confirmed by molecular genetic analysis. However, the resultant high short-term variance in reproductive success did not translate into equally high long-term variance because male dominance status was unstable. An important consequence of high but unstable short-term variance is that age cohorts will tend to be paternal sibships and social groups will be genetically substructured by age.
Differences in social relationships among community members are often explained by differences in genetic relationships. The current techniques of DNA analysis allow explicit testing of such a hypothesis. Here, we have analysed the genetic relationships for a community of wild bonobos (Pan paniscus) using nuclear and mitochondrial DNA markers extracted from faecal samples. Bonobos show an opportunistic and promiscuous mating behaviour, even with mates from outside the community. Nonetheless, we find that most infants were sired by resident males and that two dominant males together attained the highest paternity success. Intriguingly, the latter males are the sons of high-ranking females, suggesting an important influence of mothers on the paternity success of their sons. The molecular data support previous inferences on female dispersal and male philopatry. We find a total of five different mitochondrial haplotypes among 15 adult females, suggesting a frequent migration of females. Moreover, for most adult and subadult males in the group we find a matching mother, while this is not the case for most females, indicating that these leave the community during adolescence. Our study demonstrates that faecal samples can be a useful source for the determination of kinship in a whole community.
Kin selection affects many aspects of social behaviour, especially in gregarious animals in which relatives are permanently associated. In most group-living primates with complex social behaviour, females are philopatric and organized into matrilines. Models of primate social evolution assume that females in solitary primates are also organized into matrilines. We examined the genetic structure and the mating system of a population of Coquerel's dwarf lemur (Mirza coquereli), a solitary primate from Madagascar, to test this assumption. Our genetic and behavioural analyses revealed that this population of solitary individuals is indeed structured into matrilines, even though this pattern was not predicted by behavioural data. Specifically, females sharing a mitochondrial DNA haplotype were significantly clustered in space and the average genetic and geographical distances among them were negatively correlated. Not all females were philopatric, but there is no evidence for the successful settlement of dispersing females. Although not all adult males dispersed from their natal range, they were not significantly clustered in space and all of them roamed widely in search of oestrous females. As a result, paternity was widely spread among males and mixed paternities existed, indicating that scramble competition polygyny is the mating system of this species. Our data therefore revealed facultative dispersal in both sexes with a strong bias towards female philopatry in this primitive primate. We further conclude that complex kinship structures also exist in non-gregarious species, where their consequences for social behaviour are not obvious.
In many cooperatively breeding vertebrates, a dominant breeding pair is assisted in offspring care by nonbreeding helpers.
A leading explanation for this altruistic behavior is Hamilton's idea that helpers gain indirect fitness benefits by rearing
relatives (kin selection). Many studies have shown that helpers typically provide care for relatives, but relatively few have
shown that helpers provide closer kin with preferential care (kin discrimination), fueling the suggestion that kin selection
only poorly accounts for the evolution of cooperative breeding in vertebrates. We used meta-analysis to show that (i) individuals
consistently discriminate between kin, and (ii) stronger discrimination occurs in species where the benefits of helping are
greater. These results suggest a general role for kin selection and that the relative importance of kin selection varies across
species, as predicted by Hamilton's rule.
A new method is described for estimating genetic relatedness from genetic markers such as protein polymorphisms. It is based on Grafen's (1985) relatedness coefficient and is most easily interpreted in terms of identity by descent rather than as a genetic regression. It has several advantages over methods currently in use: it eliminates a downward bias for small sample sizes; it improves estimation of relatedness for subsets of population samples; and it allows estimation of relatedness for a single group or for a single pair of individuals. Individual estimates of relatedness tend to be highly variable but, in aggregate, can still be very useful as data for nonparametric tests. Such tests allow testing for differences in relatedness between two samples or for correlating individual relatedness values with another variable.
— Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis. A microsatellite-based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three-year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extra group paternity, resulted in low levels of relatedness between subordinates and non descendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.
Introduction Walter D. Koenig and Janis L. Dickinson 1. Evolutionary origins J. David Ligon and D. Brent Burt 2. Delayed dispersal Jan Ekman, Janis L. Dickinson, Ben J. Hatchwell and Michael Griesser 3. Fitness consequences of helping Janis L. Dickinson and Ben J. Hatchwell 4. Parental care, load-lightening and costs Robert G. Heinsohn 5. Matings systems and sexual conflict Andrew Cockburn 6. Sex-ratio manipulation Jan Komdeur 7. Physiological ecology Morne Du Plessis 8. Endocrinology Steven J. Schoech, S. James Reynolds and Raoul K. Boughton 9. Incest and incest avoidance Walter D. Koenig and Joseph Haydock 10. Reproductive skew Robert D. Magrath, Rufus A. Johnstone and Robert G. Heinsohn 11. Joint-laying systems Sandra L. Vehrencamp and James S. Quinn 12. Conservation biology Jeffrey R. Walters, Caren B. Cooper, Susan J. Daniels, Gilberto Pasinelli and Karen Schiegg 13. Mammalian contrasts and comparisons Andrew F. Russell Summary Steven J. Pruett-Jones Names of bird and mammal species mentioned in the text References Index.
A new method is described for estimating genetic relatedness from genetic markers such as protein polymorphisms. It is based on Grafen's (1985) relatedness coefficient and is most easily interpreted in terms of identity by descent rather than as a genetic regression. It has several advantages over methods currently in use: it eliminates a downward bias for small sample sizes; it improves estimation of relatedness for subsets of population samples; and it allows estimation of relatedness for a single group or for a single pair of individuals. Individual estimates of relatedness tend to be highly variable but, in aggregate, can still be very useful as data for nonparametric tests. Such tests allow testing for differences in relatedness between two samples or for correlating individual relatedness values with another variable.
Genetic techniques and long‐term behavioural observations were combined to investigate dispersal patterns and changes in social position in Neolamprologus pulcher, a co‐operatively breeding cichlid from Lake Tanganyika. Comparisons of genetic variance (FST) across sub‐populations demonstrated that fish were genetically more similar to individuals from proximate sub‐populations compared to individuals from distant sub‐populations. Microsatellite analyses revealed year‐long philopatry for some individuals and that other individuals dispersed to new territories and sub‐populations. Individuals appeared to disperse farther (across many territories in a sub‐population or to new sub‐populations) to achieve breeding status. Non‐breeding group members (or helpers) were observed to inherit breeding positions and male breeders were replaced faster than female breeders. These results demonstrate that important and difficult to obtain life‐history information can be obtained from genetic sampling.
and Summary
L. brichardi is a substrate brooding cichlid with facultative polygamy. The social organization was studied in the field for a 6‐week period. The mating structure was examined in detail in the laboratory. Two types of social groupings are described:
Aggregations of sexually mature but nonterritorial fish, also frequently visited by territory holders in the vicinity.
Reproductive units (families) mainly consisting of the reproducing pair members and offspring from several broods. All family members defend a common territory around the shelter site. Occasionally a male has access to two females each with a separate territory (harem).
The factors influencing mating structure were investigated in the laboratory:
Females select breeding sites rather than partners.
Without competitors for breeding sites, and with an equal or nearly equal sex ratio, harems were established nearly as often as pairs.
Young males are physically able to mate and form a harem; but they are usually prevented from doing so by more competitive (larger) males.
Competition for breeding sites is not a prime influence on harem formation, although it is of great importance in determining the composition and size of the breeding population.
Just as many pairs as harems were formed with and without predators, even though, with predators, no young survived.
In L. brichardi the formation of harems is not predominantly determined by the distribution of suitable spawning sites. The monopolization of females is only slightly influenced by the distance between their territories.
In L. brichardi it is not necessary for harem formation that the male is bigger than the female.
Behavioural protocols and data on growth rates, as well as spawning intervals, did reveal any consistent difference between pairs and harmes.
Of the variables tested, male competition for females was therefore the sole determinant of who should mate.
In the cooperatively breeding Lamprologus brichardi, helpers clearly prefer to stay in the family territory rather than leave for an aggregation of same-size young or for an unoccupied area, even when their chances of reproducing independently are superior to those in the field. Helpers usually attain independence when the breeders force them to leave the territory. Breeders' toleration of helpers depends on stage in the reproductive cycle, size of helpers and the need for helpers. Large, previously expelled helpers are reaccepted when competition is increased. In these circumstances breeders prefer their own former helpers to strange young. Three factors are ultimately important for the breeder/helper relationship: reproductive parasitism by mature helpers, eventual cannibalism on breeders' eggs and competition for shelter within the territory. A graphical model shows how the initially common interests of breeders and helpers develop divergently when helpers reach the size at which they become sexually mature and less susceptible to predation. Large helpers pay to stay. The relationship of breeders and large helpers meets the criterion of reciprocal altruism.-from Author
Most theories of social behaviour and cooperation assume that animals can recognise other individuals, but this is rarefy tested. Using Neolamprologus brichardi, a cooperatively breeding cichlid fish, we monitored behavioural responses to (1) real fish versus video images of fish; (2) mate versus neighbour and (3) video images of mate versus video image of neighbour. All tests were controlled for size and sex. Fish reacted appropriately to the playbacks, although responses to videos were not as strong as to real fish. Both males and females fought against the images of stranger and neighbour fish and they courted images of mates. These results confirm that the cooperatively breeding fish, Neolamprologus brichardi, recognises individuals based on vision and that video playbacks contain sufficient information to facilitate recognition.
Parental care in the Malawian cichlid fishPseudotropheus zebra BB is extensive and exclusively maternal; males contribute only genetic material. The costs of searching for multiple mates (in this case risk of predation on orally incubated eggs) suggested that females should be monandrous; microsatellite genetypes of seven brooding females and their young, however, reveal extensive multiple paternity in this species, with a mean of 3.8 paternal individuals per brood. Polygynandry inP. zebra is probably not maintained by selection for genetically diverse offspring; potential explanations include avoidance of inbreeding, and bet-hedging on other male characteristics that females are unable to evaluate when selecting a mate. The observed degree of multiple paternity strongly suggests that females are free to choose mates as they will, a prerequisite of many theories positing sexual selection as a key element in Malawi chichlid evolution. It should also result in elevation of effective population sizes, and thus be antagonistic to runaway evolution of male secondary sexual characteristics, but not necessarily to other modes of sexual selection.
Evaluation of evolutionary mechanisms proposed to promote cooperative behavior depends on the relative influence of the behavior
on the reproductive success of individuals, the reproductive success of the group in which they interact behaviorally, and
the degree of gene correlation among cooperators. The genetic relationship within cooperative coalitions of female red howler
monkeys was examined for three populations with different densities and growth rates. Patterns of gene correlation change
within coalitions is documented using data from the mitochondrial and nuclear genomes, and long-term census monitoring. Differences
in fecundity and infant survivorship within and between groups of unrelated (r¯=0) and related (r¯≥ 0.25) females are compared. Females that emigrate from their natal groups form coalitions with other migrant females. These
coalitions attempt to establish a territory and, once successful in producing offspring, exclude other females from feeding
resources. Females in these coalitions had different mtDNA haplotypes and a genetically estimated mean r of 0, supporting demographic data on emigration patterns indicating that these females rarely have the opportunity to form
coalitions with kin. Patterns of recruitment and rate of matriline development within social groups supported behavioral data
indicating that females actively attempt to promote their own matriline as breeders over that of other females, and that some
matrilines are more successful at this than others. Mean r among females was significantly higher in coalitions established as social groups for several generations (r¯=0.44). In these groups, females all shared the same mtDNA haplotype, and mtDNA haplotype divergence was significantly higher
between than within groups. Females in coalitions with kin had significantly higher reproductive success than females in unrelated
coalitions in all populations. This difference was not a function of coalition size, number of males, socionomic sex ratio,
or primiparity, although anecdotal evidence suggests that allomothering may compensate for inept new mothers in related coalitions
more often than in unrelated ones. Differences in territory quality could not be ruled out as a potential causal factor in
the saturated populations, but were unlikely in the low-density, growing population. There were substantial differences among
long-established coalitions in overall reproductive output in all three populations, and this was significantly correlated
with the number of breeding females. Increase in coalition size was a function of both group age and the behavioral tolerance
among females. Regardless of the underlying reasons for the patterns observed, reproductive success clearly increases with
degree of gene correlation among females within cooperative coalitions, and coalitions that recruit more daughters produce
more offspring. The nature of the cooperative relationship among group females directly influences both of these outcomes.
This is associated with substantial genetic differentiation among social groups within populations, creating conditions in
which genetic tendencies towards cooperative behavior can become tightly associated with group reproductive success.
Group size has been shown to positively influence survival of group members in many cooperatively breeding vertebrates, including the Lake Tanganyika cichlid Neolamprologus pulcher, suggesting Allee effects. However, long-term data are scarce to test how these survival differences translate into changes in group extinction risk, group size and composition. We show in a field study of 117 groups from six different colonies (three from two populations each), that group size critically influences these parameters between years. Within one year, 34% of the groups went extinct. Group size correlated positively between years and large groups did not go extinct. The latter were more likely to contain small helpers the subsequent year, which is a cumulative measure of the previous months' reproductive success. Finally, there was a tendency that large groups were more likely to contain a breeding male and female still a year after the first check. The breeder male size, breeder female size, and largest helper size did not influence these parameters, and also did not correlate with the sizes of these categories of fish after one year. This suggests that group size, and not the body size or fighting ability of group members, was the critical variable determining the success of groups. In total, seven groups had fused with other groups between years. To our knowledge, this is the first study showing long-term benefits of large group size in a cooperatively breeding fish. We discuss the importance of differential survival and dispersal of group members for the demonstrated group size effects.
It has recently been argued that the paradox of helping behavior in birds has been solved (73). This optimism may be premature. I argue that there is no obvious dichotomy between cooperative societies based on natal philopatry and the formation of extended families, and those formed via recruitment of unrelated individuals into coalitions. Tests of the effect of helping behavior suggest that kinship may have been overemphasized for male helpers but underestimated for females. The first studies applying molecular techniques to resolve genealogy in these societies suggest that reproductive sharing occurs commonly across all types of social organization. Incest avoidance may be an important constraint on sharing in families, but molecular techniques have thus far been inappropriate to assess its importance. The interests of males and female helpers may be quite different because females often have less opportunity to inherit a territory vacancy on the death of the breeder, less opportunity to court mates by helping them, and less opportunity to share reproduction without perturbing the size of the brood. We still have only a weak understanding of sex biases in helping behavior.
‘Helping’ in birds and mammals involves seemingly altruistic behaviour. In the cichlid fish Lamprologus birchardi helpers are usually young of former broods staying in their parents' territories and participating in all kinds of parental duties (Broodcare, territory maintenance and defence). The discovery of helpers in fish offered the chance of attempting an extensive analysis of potential costs and benefits influencing the evolution of helpers in a vertebrate. Three factors proved to be of major importance in the cost-benefit analysis of helping as opposed to leaving for family-independent nonreproductive aggregations. Due to investment and to their rank within a family's hierarchy, helpers grow at a slower rate than non-helpers. This cost is compensated for by (i) a lower mortality risk to helpers caused by their access to a defended shelter and by protection afforded by bigger family members, and (ii) a positive contribution by helpers to the future reproductive success of their parents: females with helpers produce bigger clutches and consequently more free-swimming fry (=siblings). Other variables, such as the helpers' influence on the relative breeding success of their parents, broodcare experience through helping, the chances of territory take-over, parasitism of parents' reproduction and cannibalism are of minor importance. Similar social organizations in other fish are discussed with respect to their ecology and are compared with cooperatively breeding birds and mammals.
The ‘pay-to-stay hypothesis’ proposes that subordinate group members help dominants in order to be tolerated in the territory. Accordingly, helpers should be punished if they are not helping sufficiently and should increase helping behaviour thereafter. We tested whether helping and social behaviours of group members of the cooperatively breeding cichlid Neolamprologus pulcher change according to these predictions. A focal helper was experimentally prevented from helping to defend the territory against a conspecific intruder by depriving it of the information that an intruder was present. At the same time the other group members witnessed both the intruder and the ‘passive’ focal helper. When a helper was prevented from providing help, the other group members compensated by increasing defence of the territory, which suggests that the contribution of the passive helper was beneficial. As predicted by the pay-to-stay hypothesis, helpers increased helping behaviour after being prevented from helping. However, we found no indications that dominants punished the focal helper for not having helped before. Punishment may not be measurable, though, because of an appeasement function of helping behaviour. In accordance with this hypothesis, agonistic interactions between focal helpers and dominants were reduced when helpers helped. Apparently, helpers prevent punishment by increasing helping and submissive behaviours. Our data support the pay-to-stay hypothesis and suggest a new mechanism for the regulation of cooperative investment by subordinates: pre-emptive appeasement of dominants through helping and submissive behaviour.
Female intra-sexual competition plays an important role in the settlement process during pair or harem formation and in established harems of Lamprologus ocellatus , a small snail shell inhabiting cichlid from Lake Tanganyika. Larger females settle first and this could partly be due to male preference for larger females as shown in simultaneous choice tests but is also due to dominance of the larger female. Smaller females were unable to settle close to a larger one. Even when snail shells were not limiting the smaller was either unable to settle or had to settle at a considerable distance. This effect was independent of prior residence. Intense female-female aggression suggests that close settlement is disadvantageous to females. Genetic analyses of maternity using microsatellite length polymorphism at five loci showed a reproductive skew between females in a harem. Additionally, it proved brood mixing in aquaria as well as in the field. Brood mixing can be detrimental to female breeding success through interbrood cannibalism if size difference of juveniles amounts to 5 mm. Territoriality of juveniles, shown even between same-sized siblings, may cause indirect mortality through earlier dispersal of young. Females rejected experimentally added larger juveniles but accepted young smaller than their own fry. Acceptance of smaller juveniles could be advantageous through a dilution of predator attacks but it also appears to induce costs since females with young at the shell do not rear another brood. Large median distances of 91 cm maintained aggressively between breeding females in the field may serve to minimize the adverse effects of breeding in a harem.
Genealogical relatedness is thought to be an important causal factor in the evolution of cooperation. We inferred relatedness on the basis of 11 blood protein markers using the Queller and Goodnight index of relatedness in a macaque population with long-term demographic records. This estimate reflected independently determined pedigree relationships in our data set. Mean relatedness among all members of a social group was 0.10 but much higher levels of relatedness (0.30-0.47) were found among the members of matrilineal families with a high or intermediate social rank. Groups of dispersing males that had been born into the same social group were sometimes closely related (0.43 and 0.58), but they could also be less related (0.08). We found that the pattern of distribution of relatedness was associated with gene flow and differential reproduction in males, rather than with group fission and the presence of geographical barriers.
The ecological constraints hypothesis is widely accepted as an explanation for the evolution of delayed dispersal in cooperatively breeding birds. Intraspecific studies offer the strongest support. Observational studies have demonstrated a positive association between the severity of ecological constraints and the prevalence of cooperation, and experimental studies in which constraints on independent breeding were relaxed resulted in helpers moving to adopt the vacant breeding opportunities. However, this hypothesis has proved less successful in explaining why cooperative breeding has evolved in some species or lineages but not in others. Comparative studies have failed to identify ecological factors that differ consistently between cooperative and noncooperative species. The life history hypothesis, which emphasizes the role of life history traits in the evolution of cooperative breeding, offers a solution to this difficulty. A recent analysis showed that low adult mortality and low dispersal predisposed certain lineages to show cooperative behaviour, given the right ecological conditions. This represents an important advance, not least by offering an explanation for the patchy phylogenetic distribution of cooperative breeding. We discuss the complementary nature of these two hypotheses and suggest that rather than regarding life history traits as predisposing and ecological factors as facilitating cooperation, they are more likely to act in concert. While acknowledging that different cooperative systems may be a consequence of different selective pressures, we suggest that to identify the key differences between cooperative and noncooperative species, a broad constraints hypothesis that incorporates ecological and life history traits in a single measure of 'turnover of breeding opportunities' may provide the most promising avenue for future comparative studies. Copyright 2000 The Association for the Study of Animal Behaviour.
Reproductive-skew theory can be broadly divided into transactional models, in which reproduction is shared among group members in return for some fitness benefit, and tug-of-war models, in which reproductive sharing arises solely from an inability of each group member to fully control the others. For small-colony social insects in which complete reproductive control by a single individual is plausible, transactional-concession models account, better than any other existing model, for observed relationships between each of the dependent variables of skew, changes in reproductive partitioning over time, group size, and within-group aggression, and each of the predictor variables of genetic relatedness, ecological constraints on solitary breeding, and benefits of group living. An extension of transactional-concession models via the "workers-as-a-collective-dominant" model potentially offers new insights into some of the most striking reproductive patterns in large-colony eusocial Hymenopteran species, from the loss of worker capacity to produce female offspring to patterns of skew and aggression in polygynous societies.
Although there is mounting evidence that speciation can occur under sympatric conditions, unambiguous examples from nature are rare and it is almost always possible to propose alternative allopatric or parapatric scenarios. To identify an unequivocal case of sympatric speciation it is, therefore, necessary to analyse natural settings where recent monophyletic species flocks have evolved within a small and confined spatial range. We have studied such a case with a cichlid species flock that comprises five Tilapia forms endemic to a tiny lake (Lake Ejagham with a surface area of approximately 0.49 km2) in Western Cameroon. Analysis of mitochondrial D-Loop sequences shows that the flock is very young (approximately 10(4) years) and has originated from an adjacent riverine founder population. We have focused our study on a particular pair of forms within the lake that currently appears to be in the process of speciation. This pair is characterized by an unique breeding colouration and specific morphological aspects, which can serve as synapomorphic characters to prove monophyly. It has differentiated into a large inshore and a small pelagic form, apparently as a response to differential utilization of food resources. Still, breeding and brood care occurs in overlapping areas, both in time and space. Analysis of nuclear gene flow on the basis of microsatellite polymorphisms shows a highly restricted gene flow between the forms, suggesting reproductive isolation between them. This reproductive isolation is apparently achieved by size assortative mating, although occasional mixed pairs can be observed. Our findings are congruent with recent theoretical models for sympatric speciation, which show that differential ecological adaptations in combination with assortative mating could easily lead to speciation in sympatry.
In cooperatively breeding vertebrates, nonbreeding helpers raise young produced by dominant breeders. Although the evolution
of cooperative breeding has often been attributed primarily to kin selection (whereby individuals gain “indirect” benefits
to their fitness by assisting collateral relatives), there is increasing evidence that helpers can be unrelated to the young
they are raising. Recent studies also suggest that the indirect benefits of cooperative behavior may often have been overestimated
while the direct benefits of helping to the helper's own fitness have probably been underestimated. It now seems likely that
the evolutionary mechanisms maintaining cooperative breeding are diverse and that, in some species, the direct benefits of
helping may be sufficient to maintain cooperative societies. The benefits of cooperation in vertebrate societies may consequently
show parallels with those in human societies, where cooperation between unrelated individuals is frequent and social institutions
are often maintained by generalized reciprocity.
Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis. A microsatellite-based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three-year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extragroup paternity, resulted in low levels of relatedness between subordinates and nondescendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.
Spotted hyenas (Crocuta crocuta) are gregarious carnivores that live in multigenerational social groups, called clans, containing one to several matrilines. Members of multiple matrilines within a clan cooperate during dangerous interactions with inter- and intraspecific competitors. The evolution of cooperation may be influenced by relatedness between individuals, which in turn is influenced by reproductive skew and mate choice, dispersal and territorial behaviours. Behavioural data exist for spotted hyenas, but corresponding data on patterns of relatedness are unavailable; this lack of data makes it difficult to assess the relative importance of selection pressures favouring cooperative behaviour within and among groups. Therefore we conducted a longitudinal analysis of relatedness within a single large clan of spotted hyenas, as well as a cross-sectional analysis of relatedness among hyenas from multiple clans. Within a clan, patterns of relatedness reflected known pedigree relationships, and relatedness was higher within than among matrilines, even across generations. Although mean within-matriline relatedness varied among matrilines, it did not decline with matriline rank. On average, clan members were not related closely, due to high levels of male-mediated gene flow among clans, and relatedness declined very slightly across clan borders. Low mean relatedness within clans suggests that spotted hyenas cooperate with unrelated clan-mates against close paternal kin in other clans. Our data also suggest that spotted hyenas must derive large net direct fitness benefits from group living and cooperation.
The sweat bees (Family Halictidae) are a socially diverse taxon in which eusociality has arisen independently numerous times. The obligate, primitively eusocial Lasioglossum malachurum, distributed widely throughout Europe, has been considered the zenith of sociality within halictids. A single queen heads a colony of smaller daughter workers which, by mid-summer, produce new sexuals (males and gynes), of which only the mated gynes overwinter to found new colonies the following spring. We excavated successfully 18 nests during the worker- and gyne-producing phases of the colony cycle and analysed each nest's queen and either all workers or all gynes using highly variable microsatellite loci developed specifically for this species. Three important points arise from our analyses. First, queens are facultatively polyandrous (queen effective mating frequency: range 1-3, harmonic mean 1.13). Second, queens may head colonies containing unrelated individuals (n = 6 of 18 nests), most probably a consequence of colony usurpation during the early phase of the colony cycle before worker emergence. Third, nonqueen's workers may, but the queen's own workers do not, lay fertilized eggs in the presence of the queen that successfully develop into gynes, in agreement with so-called 'concession' models of reproductive skew.