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Paternal behaviour in wild guinea pigs: A comparative study in three closely related species with different social and mating systems
Journal of Zoology
Abstract
In most species, females invest more in their offspring than males. In mammals, this also holds true after the birth of young since only mothers can lactate and fathers are thus more likely to desert and seek additional mating opportunities. These opportunities are largely dependent on resource distribution and the resulting distribution of females. The emerging social and mating systems of different species give rise to different benefits of investment in paternal care. Paternal care should have evolved in relation to the frequency of losing paternities to other males. Hence, in species living in one-male systems with little opportunity for female extra-pair copulations, paternal care should be more common than in those species living in multi-male groups. The guinea pigs (Caviinae) comprise closely related species exhibiting different social organizations and mating systems. The amount of paternal behaviour and offspring-directed aggression was investigated in three species kept under laboratory conditions: the polygynous Cavia aperea, the promiscuous Galea musteloides and a newly described monogamous species (Galea monasteriensis sp. nov.). All animals were kept in groups of one adult male and one adult female with their non-weaned offspring. Cavia aperea as well as G. monasteriensis males showed a high incidence of paternal behaviour, which consisted primarily of playing with offspring and grooming them. In contrast, G musteloides males never engaged in paternal behaviour but directed more aggressive behaviour towards their offspring. Mating with multiple partners and multiple paternities are common in G musteloides whereas in the former two species there is a much higher certainty of paternity. We conclude that paternal behaviour in guinea pigs probably co-evolved in alignment with the certainty of paternity that males of a species encounter under natural conditions.
... Although typically displayed by the females, male care occurs with some frequency in mammals [2], including primates, perissodactyls, carnivores and rodents [3,4]. Among species of rodents, the father may exhibit huddling with the offspring, active grooming and retrieval, nest maintenance and defense, and food provision [5,6]. Previous studies in prairie voles (Microtus ochrogaster), California mice (Peromyscus californicus), Mongolian gerbils (Meriones unguiculatus), Djungarian hamsters (Phodopus campbelli), dwarf hamsters (Phodopus roborovskii), volcano mice (Neotomodon alstoni), Bolivian yellow-toothed cavies (Galea monateriensis), wild cavies (Cavia aparea), and rats (Rattus sp.), highlight considerable variation across species in the quantity and quality of parental care provided by the males [3,5,6,7,8]. ...
... Among species of rodents, the father may exhibit huddling with the offspring, active grooming and retrieval, nest maintenance and defense, and food provision [5,6]. Previous studies in prairie voles (Microtus ochrogaster), California mice (Peromyscus californicus), Mongolian gerbils (Meriones unguiculatus), Djungarian hamsters (Phodopus campbelli), dwarf hamsters (Phodopus roborovskii), volcano mice (Neotomodon alstoni), Bolivian yellow-toothed cavies (Galea monateriensis), wild cavies (Cavia aparea), and rats (Rattus sp.), highlight considerable variation across species in the quantity and quality of parental care provided by the males [3,5,6,7,8]. Functionally, this variation seems associated with several factors, including the prevalent mating system [3,6]. ...
... Previous studies in prairie voles (Microtus ochrogaster), California mice (Peromyscus californicus), Mongolian gerbils (Meriones unguiculatus), Djungarian hamsters (Phodopus campbelli), dwarf hamsters (Phodopus roborovskii), volcano mice (Neotomodon alstoni), Bolivian yellow-toothed cavies (Galea monateriensis), wild cavies (Cavia aparea), and rats (Rattus sp.), highlight considerable variation across species in the quantity and quality of parental care provided by the males [3,5,6,7,8]. Functionally, this variation seems associated with several factors, including the prevalent mating system [3,6]. Specifically, males in mammalian species exhibiting a predominantly monogamous mating system provide extended paternal care, implying that certainty of paternity plays a role [8]. ...
Parents in many animal species provide care to their offspring as a mechanism to enhance their own fitness. In mammals, this behavior is expressed mostly by the females, but also by males of some species. Proximally, rates of paternal offspring care have been linked to organizational and activational effects of testosterone. Specifically, intrauterine position of male fetuses is associated with differential exposure to testosterone, leading to development of males with different levels of masculinization (assessed through differences in the length of the anogenital distance (AGD). The relative roles played by organizational and activational effects of testosterone on male parental care remain unclear. In this study, we aimed to determine if male sex-biased uterine environment and testosterone levels across the breeding period explain variation in paternal care in the social rodent, Octodon degus. Neither quantity (time with the offspring) nor quality (frequency of grooming and retrieving) of paternal care was affected by male sex-biased uterine environment, nor did paternal care significantly differ across the different stages of male reproduction. In contrast, paternal care was associated with maternal care. Quantity of male care decreased with increasing quantity of maternal care, and quality of male care increased with increasing quality of maternal care. While serum testosterone did not differ between males with different sex-biased uterine environment, male testosterone tended to increase during mating and decrease when pregnant females or offspring were present.
... A origem da cobaia, o local da domesticação e a época em que aconteceu, também não são pontos de consenso entre os autores. C. aperea (King, 1956;Rood, 1972;Eisenberg, 1974;Sachser, 1998;Künzl e Sachser, 1999;Asher e Sachser, 2000;Hohoff et al., 2000;Asher e Sachser, 2001;Hohoff, 2002;Künzl et al., 2002;Asher et al., 2004;Adrian et al., 2005), C. tschudii (Nehring, 1889em Weir, 1974Ortiz, 2003;Spotorno et al. , 2004) e C.fulgida (Thomas, 1901, em Weir, 1974Ortiz, 2003) foram apontadas como espécies irmãs da cobaia, derivadas de um ancestral comum dela separadas por um processo de domesticação. ...
... Há contudo uma diferença interessante entre cobaias e preás em relação ao cuidado paterno. Em cobaias, os pais quase não exibem comportamentos de cuidado aos filhotes (apesar de serem tolerantes e investigarem os filhotes pelo mesmo tempo que investigam a fêmea) e o pouco que fazem é constante durante as 4 primeiras semanas de vida (Beisiegel, 1993 (Adrian et al., 2005). Os autores classificam os saltos com contorção como brincadeira social. ...
... Salto com contorção (Messias, 1995;frisky hops, Rood, 1972, Lacher, 1981 contact-hopping e simultaneos hopping, Adrian et al., 2005). São pequenos e repetidos saltos para cima, tirando simultaneamente as quatro patas do chão, com o corpo e a cabeça torcidos para o lado. ...
... Further, adult females are less tolerant of unrelated pups than are females of the polygynous wild cavy, Cavia aperea (Hennessy et al., 2006). As in other monogamous species, G. monasteriensis males exhibit relatively elevated levels of paternal care (Adrian et al., 2005) and suppressed measures of reproductive capacity (e.g., testis weight significantly lower than in G. musteloides), and there is a reversed sexual dimorphism with females being about 9% heavier than males (Hohoff et al., 2002). In tests of mate choice by females, findings contrasted sharply with those described above for the promiscuous G. musteloides. ...
... The male bonding partner could respond with an increased share of parental care. This is a conceivable explanation here, since male G. monasteriensis engage in paternal behaviors in contrast to the closely related but promiscuous G. musteloides (Adrian et al., 2005). It is not clear, how-ever, whether direct paternal care increases the fitness of G. monasteriensis offspring. ...
... This species can be characterized as rather solitary in regards to its social organization and promiscuous in terms of its mating system. Consequently, males have a low certainty of paternity and do not engage in paternal behaviors (Adrian et al., 2005). Additionally, in G. musteloides, it has been shown that females benefit from mating with multiple partners-which they actively solicitby increased survival of the offspring (Keil and Sachser, 1998). ...
We examined the possible existence of, and female contributions to, pair bonds, as well as the relation of social preference to mating selectivity, in a recently identified wild guinea pig, the Muenster yellow-toothed cavy (Galea monasteriensis). In Experiment 1, females housed for approximately 20 days in an apparatus in which they could choose to approach and interact with unfamiliar males typically exhibited a robust preference for one of two available males. DNA fingerprinting revealed a strong association between female choice and paternity. Experiment 2 examined the influence of the removal and return of the female on male plasma cortisol levels and behavior in established breeding pairs. A 2-h period of separation in the home enclosure elevated male cortisol levels. Return of the female to the home enclosure reduced male cortisol levels 2 h later, whereas continued separation did not. Reunion in either the home or novel enclosure increased socio-positive and courtship/sexual behavior, as well as time spent in proximity of the partner. Together, these results provide evidence for a substantial female influence on pair bond formation and maintenance in G. monasteriensis and further support for the existence of social and sexual monogamy in this species.
... 10 Additionally, there are conflicting reports as to the presence of auditory sex differences in guinea pigs, which exhibit variation in the presence or absence of social monogamy and/or parental care. 10,17 This suggests that it is possible that sex-based auditory differences might be related to the degree of difference in parental care by the sexes. Given the high degree of parental and alloparental care exhibited by male prairie voles, they may serve as an ideal species to further examine the possibility of this relationship. ...
... 2,3 It would be interesting to directly compare similar measures and potential sex differences to other species with similar parental care and breeding strategies such as Mongolian gerbils and guinea pigs. 12,17 These results are also consistent with broad tuning of auditory responses found in other rodents, such as Onychomys leucogaster (northern grasshopper mice, broad sensitivity from 8 to 24 kHz), 48 which are consistent with the matched filter hypothesis that proposes that sensory systems evolve to detect the most ecologically relevant stimuli. 49 Male prairie voles did weigh significantly more than females; however, increased mass does not translate to overall larger heads or pinna. ...
The hearing abilities of mammals are impacted by factors such as social cues, habitat, and physical characteristics. Despite being used commonly to study social behaviors, hearing of the monogamous prairie vole (Microtus ochrogaster) has never been characterized. In this study, anatomical features are measured and auditory brainstem responses (ABRs) are used to measure auditory capabilities of prairie voles, characterizing monaural and binaural hearing and hearing range. Sexually naive male and female voles were measured to characterize differences due to sex. It was found that prairie voles show a hearing range with greatest sensitivity between 8 and 32 kHz, binaural hearing across interaural time difference ranges appropriate for their head sizes. No differences are shown between the sexes in binaural hearing or hearing range (except at 1 kHz), however, female voles have increased amplitude of peripheral ABR waves I and II and longer latency of waves III and IV compared to males. The results confirm that prairie voles have a broad hearing range, binaural hearing consistent with rodents of similar size, and differences in amplitudes and thresholds of monaural physiological measures between the sexes. These data further highlight the necessity to understand sex-specific differences in neural processing that may underly variability in responses between sexes.
... The cavy Cavia aperea Erxleben, 1777, is widely considered to be the closest living relative species to the domestic cavy. Some authors even consider the domestic cavy (designated here as C. aperea f. porcellus) and C. aperea to belong to the same species (Sachser 1998;Künzl & Sachser 1999;Adrian et al. 2005;Kemme et al. 2009). Others, based on molecular data, maintain that, while closely related, C. aperea and C. porcellus are actually distinct species (Bonatto et al. 1995;Spotorno et al. 2004). ...
... The behavioral repertoires of the wild and domestic species are very similar. In both species there are strong mother-infant and male-female bonds (Sachser 1998;Künzl & Sachser 1999;Sachser et al. 1999;Asher et al. 2008), allosuckling behavior (Monticelli & Ades 2003;Takamatsu et al. 2003) and limited paternal care of pups (Beisiegel 1993;Sachser 1998;Monticelli & Ades 2003;Adrian et al. 2005). C. porcellus, however, displays greater tolerance to conspecifics and less wariness toward its human handlers than C. aperea (Rood 1972;Künzl & Sachser 1999). ...
Comparisons of wild (Cavia aperea) and domestic (C. porcellus) cavies promote an understanding of the physiological and behavioral effects of domestication. The richness and peculiarities of Cavia acoustic repertoires encourage the use of this model for testing how domestication alters repertoires and the physical structure of calls. We present a comparison between alarm and courtship calls of domestic and two populations of wild cavies from different geographic regions, one of them with a short-term captivity history of 25 generations. We found significant differences between domestic and wild cavies in both calls, particularly in temporal parameters, and only spectral differences between two wild populations in alarm calls. There were also differences in the frequency of emission of calls: alarm calls were more frequent in the wild and courtship calls were more frequent in the domestic species. Our results suggest that domestication has influenced the temporal parameters of both alarm and courtship calls of C. porcellus, but not the spectral parameters that, instead, may be influenced by environment or population factors.
... Males take part in parental care either as sole caregivers (particularly common in fishes; Reynolds et al., 2002) or alongside with females. Male participation in parental care can be found in a surprisingly diverse array of animal groups and there are marked differences among species in the extent of parental care provided by the male, including in insects (Gilbert & Manica, 2010), amphibians (Duellman & Trueb, 1986), fishes (Mank et al., 2005), birds (Webb et al., 2010) and mammals (Adrian et al., 2005). However, social and ecological factors responsible for these differences remain contentious (Ridley, 1978;Gross & Sargent, 1985;Ketterson & Nolan, 1994;Beck, 1998;Tallamy, 2000;Burley & Johnson, 2002;Szé kely et al., 2006;Alonzo, 2009). ...
... Social mating system was revealed to be an important correlate of male's contribution to parental care across species (Wright, 1998;Adrian et al., 2005). For example, in polygynous species, it is mostly the female who provides parental care, whereas in monogamous species, parental care is usually shared by the breeding pair (Verner & Willson, 1969;Szé kely et al., 2007). ...
Parental care provided by males occurs in a diverse array of animals and there are large differences among species in its extent compared with female care. However, social and ecological factors responsible for interspecific differences in male's share of parental duties remain unclear. Genetic fidelity of females has been long considered important. Theory predicts that females should receive more help from their mates in raising the offspring in species with high genetic fidelity. Using avian incubation behaviour as a model system, we confirmed this prediction. The extent of male's help during incubation increased with decreasing rate of extra-pair paternity across species (22 species of socially monogamous songbirds from 13 families; male's share of incubation ranged from 6% to 58%), even after accounting for covariates, biases in species selection and intraspecific variability. Moreover, this result was not sensitive to two different phylogenies and branch length estimates. We suggest that our findings support the notion, backed by theory, that genetic fidelity is an important factor in the evolution of male parental care. We offer several behavioural scenarios for the coevolution between male's share of parental duties and the genetic mating system.
... Moreover, males never exhibited aggression to the young. Qualitatively, male degus seemed parentally intermediate between more paternal males of biparental and cooperatively breeding rodents [66][67][68], and the less paternal males of more promiscuous or less social species [10,67,69,70]. Quantitatively, care by male degus did not occur only occasionally. ...
... To some extent, these findings are consistent with the hypothesis that males exhibit offspring care even if this activity has marginal fitness consequences to offspring [3]. Paternal care might be expected if the probability for future breeding attempts is low in males [69]. The reproductive biology of degus supports that this might be the case. ...
Males are expected to assist their mates whenever this behaviour raises survival of offspring with little expense in terms of mating opportunities. At a more proximate level, cortisol and testosterone hormones seem involved in the expression of parental care in mammals. We examined the consequences to postnatal offspring development and survival of the males' presence in the social rodent, Octodon degus. Offspring quality and quantity, and maternal condition of females were contrasted among females rearing their litters in the presence of the sire, females breeding in the presence of a non-breeding female, and females breeding solitarily. We related these differences to variation in parental behaviour and plasma levels of testosterone and cortisol. Twenty two females and their litters were studied under constant conditions of adult density, nest availability, food availability, and breeding experience. Males huddled over and groomed offspring. However, neither the number nor the mass of pups from dams that nested with the sire differed from those recorded to breeding females that nested with a non-breeding female and females that nested solitarily. Body weight loss and associated levels of plasma cortisol in dams nesting with the sire were similar to those of solitary females, but higher than mothers nesting with a non-breeding female. Thus, male care had no consequences to offspring, and seemed detrimental to breeding females. Circulating levels of cortisol and total testosterone were either poor (mothers) or no (fathers, non-breeding females) predictors of parental care.
... The cavy Cavia aperea Erxleben, 1777, is widely considered to be the closest living relative species to the domestic cavy. Some authors even consider the domestic cavy (designated here as C. aperea f. porcellus) and C. aperea to belong to the same species (Sachser 1998;Künzl & Sachser 1999;Adrian et al. 2005;Kemme et al. 2009). Others, based on molecular data, maintain that, while closely related, C. aperea and C. porcellus are actually distinct species (Bonatto et al. 1995;Spotorno et al. 2004). ...
... The behavioral repertoires of the wild and domestic species are very similar. In both species there are strong mother-infant and male-female bonds (Sachser 1998;Künzl & Sachser 1999;Sachser et al. 1999;Asher et al. 2008), allosuckling behavior (Monticelli & Ades 2003;Takamatsu et al. 2003) and limited paternal care of pups (Beisiegel 1993;Sachser 1998;Monticelli & Ades 2003;Adrian et al. 2005). C. porcellus, however, displays greater tolerance to conspecifics and less wariness toward its human handlers than C. aperea (Rood 1972;Künzl & Sachser 1999). ...
A comparação entre cobaias (Cavia porcellus) e preás (Cavia aperea) fornece dados relevantes para se entender o processo de domesticação (Künzl e Sachser, 1999). No presente trabalho, foram registradas e analisadas sonograficamente (l) a vocalização de alerta, drr, em cobaias e em duas amostras de preás, uma observada em Münster (Alemanha), constituída de animais provenientes da Argentina, e outra constituída de animais provenientes de Itu (São Paulo) e (2) a vocalização de côrte, purr, em cobaias e preás de Münster. Encontrou-se diferenças significativas entre C. porcellus e ambas as populações de C. aperea nos parâmetros temporais do drr (duração dos pulsos e dos intervalos entre eles e taxa de emissão) assim como diferenças significativas entre as populações de preás de Münster e de Itu (freqüências mínima e máxima da fundamental e freqüência máxima do chamado). No caso do purr, também houve diferenças significativas nos parâmetros temporais das espécies. Estes resultados demonstram a influência da domesticação e de fatores ecotípicos sobre a comunicação vocal e podem, juntamente com a análise sonográfica dos chamados de outras espécies do gênero Cavia, servir para resolução de questões filogenéticas deste grupo. Estudos com "playbacks" cruzados poderão eventualmente mostrar em que medida as diferenças de vocalização afetam o comportamento social e reprodutivo dos animais. Dissertação (Mestrado).
... In both species, C. porcellus and C. aperea, as in most mammals, mothers are the main caregivers, but allosuckling also occurs among females from the same social group (Takamatsu, Tokumaru & Ades, 2003). Males are very tolerant towards pups and eventually display frisk hops in interaction with them, but do not provide direct care (Beisiegel, 1993;Adrian, Brockmann, Hohoff et al., 2005). King (1956), observing guinea pigs in a "semi-natural" environment, reported that the precocious pups were born in natural shelters on the ground. ...
... The mating system does not seem to impact this relationship. This is not so surprising because the difference between promiscuous and polygynous mating systems is only expected to impact paternal allocation ( Adrian et al., 2005). As the degree of paternity certainty is lower in promiscuous species than in polygynous species, promiscuous fathers should allocate less than polygynous fathers ( Wright & Cotton, 1994), whereas such differences are not expected for maternal allocation. ...
Early survival is highly variable and strongly influences observed population growth rates in most vertebrate populations. One of the major potential drivers of survival variation among juveniles is body mass. Heavy juveniles are better fed and have greater body reserves, and are thus assumed to survive better than light individuals. In spite of this, some studies have failed to detect an influence of body mass on offspring survival, questioning whether offspring body mass does indeed consistently influence juvenile survival, or whether this occurs in particular species/environments. Furthermore, the causes for variation in offspring mass are poorly understood, although maternal mass has often been reported to play a crucial role. To understand why offspring differ in body mass, and how this influences juvenile survival, we performed phylogenetically corrected meta-analyses of both the relationship between offspring body mass and offspring survival in birds and mammals and the relationship between maternal mass and offspring mass in mammals. We found strong support for an overall positive effect of offspring body mass on survival, with a more pronounced influence in mammals than in birds. An increase of one standard deviation of body mass increased the odds of offspring survival by 71% in mammals and by 44% in birds. A cost of being too fat in birds in terms of flight performance might explain why body mass is a less reliable predictor of offspring survival in birds. We then looked for moderators explaining the among-study differences reported in the intensity of this relationship. Surprisingly, sex did not influence the intensity of the offspring mass–survival relationship and phylogeny only accounted for a small proportion of observed variation in the intensity of that relationship. Among the potential factors that might affect the relationship between mass and survival in juveniles, only environmental conditions was influential in mammals. Offspring survival was most strongly influenced by body mass in captive populations and wild populations in the absence of predation. We also found support for the expected positive effect of maternal mass on offspring mass in mammals (rpearson = 0.387). As body mass is a strong predictor of early survival, we expected heavier mothers to allocate more to their offspring, leading them to be heavier and so to have a higher survival. However, none of the potential factors we tested for variation in the maternal mass–offspring mass relationship had a detectable influence. Further studies should focus on linking these two relationships to determine whether a strong effect of offspring size on early survival is associated with a high correlation coefficient between maternal mass and offspring mass.
... Paternal care has been observed in several species of guinea pigs. According to Adrian et al. (2005), allogrooming and playful paternal-infant interactions were detectable in the monogamous Galea monasteriensis and polygynous harem-living Cavia aperea, but not in the promiscuous Galea musteloide, which, rather, directed aggressive behavior towards offspring. Presumably, differences among species are influenced by differences in dispersal rate, mating possibilities, and associated certainty of paternity. ...
The scientific interest in caviomorph rodents as possible animal models for social and affective neuroscience is increasing in a remarkable way. The present contribution reviews the literature on the social behavior of caviomorph species, with an emphasis on domestic guinea pigs and Octodon degus. After providing an overview of the developmental milestones, we present current laboratory-based studies on the strength of social bonds, sensitivity to social environment, and the developmental and epigenetic factors involved in the expression of social behavior. Finally, we discuss possible lines of research to broaden our knowledge of the social behavior of these promising animal models.
Keywords: degus; epigenetic; guinea pigs; social behaviour; social bonding
... Females avoid one another (Asher et al. 2008) or interact aggressively (Rood 1972) and do not provide communal care (Rood 1972). In contrast, males provide care to offspring (Adrian et al. 2005), possibly explaining why the presence of an adult male reduces the onset of puberty in females by about 30 days (Trillmich et al. 2006. To date, no one has determined if group size and reproductive success are correlated in naturally occurring populations of cavies. ...
... In both species, C. porcellus and C. aperea, as in most mammals, mothers are the main caregivers, but allosuckling also occurs among females from the same social group (Takamatsu, Tokumaru & Ades, 2003). Males are very tolerant towards pups and eventually display frisk hops in interaction with them, but do not provide direct care (Beisiegel, 1993;Adrian, Brockmann, Hohoff et al., 2005). King (1956), observing guinea pigs in a "semi-natural" environment, reported that the precocious pups were born in natural shelters on the ground. ...
When separated from their mother, wild and domestic cavy pups emit high-pitched whistles. Whistles are also emitted only by the domestic species in response to food-associated stimuli. We compared isolation whistles (IS) emitted by guinea pig pups separated from their mothers to the food-anticipation whistles (FA) emitted by the same adult individuals in response to a feeding routine. Results revealed no significant differences in the structure of the IS and FA whistles, but showed ontogenetic changes along the period. Results are discussed both in relation to the physiological mechanisms controlling whistle vocalizations and their evolutionary origin in the cavies repertoire.
Keywords: isolation call, whistle, domestication, food-associated call, parental behavior, bioacoustics
... Sexual selection, social environment, and ambient environment have been proposed to explain variation in the extent of cooperation between parents (7,(12)(13)(14). First, cooperation between parents should decrease with the intensity of sexual selection (10,15,16), and a reason for this reduction may be that sexual selection favors the sex with higher variance in mating success to reduce his (or her) care provisioning (17)(18)(19). Moreover, high mating effort might further decrease the ability of the sex under stronger sexual selection to contribute to parental care (20). ...
Significance
Parents in many animal species care for their offspring. In some species, males care more; in other species, females care more; in still other species, the contribution of the sexes is equal. However, we do not know what explains these differences among species. Using the most comprehensive analyses of parental care to date, here we show that parents cooperate more when sexual selection is not intense and the adult sex ratio of males to females is not strongly skewed. However, the degree of parental cooperation is unrelated to harshness and predictability of the ambient environment during the breeding season. Our work therefore suggests that several types of parental care may coexist in a given set of ambient environment.
... In the present study the role of the father representing a 'security-giving and arousal-reducing structure' to the isolated guinea pig pup was examined. Although adult male domestic guinea pigs (and other species of Caviinae) may be indifferent or show simple paternal behavior (playing with offspring and grooming them; Adrian et al., 2005;Beisiegel, 1993) to pups or juveniles, they have an influence on pups' behavioral development. Males raised singly or with a female are more prone to engage in very serious, escalated fighting, with other males than colony reared individuals (Sachser, 1986). ...
... However, in some species parental care is provided by both sexes. Such biparental care can be found in insects [3], amphibians [4], fishes [5], birds [6,7], and mammals [8]. In biparental species, contribution by each sex varies across species, which is also true for birds [7]. ...
Male contribution to parental care varies widely among avian species. Yet the reasons for this variation, as well as its consequences, are still unclear. Because the amount of care provided by one sex is ultimately constrained by the time available for energy acquisition, contribution by the other sex should increase when overall parental workload is high. We tested this prediction by analyzing male contribution to incubation in 528 populations of 320 species of passerines, where females usually devote more time to incubation than males. Our worldwide sample included species with female-only parental care (the male is not present), incubation feeding (the male feeds the incubating female), and shared incubation (both sexes incubate the eggs).
Overall nest attentiveness was greatest in species with shared incubation followed by species with incubation feeding and lowest in species with female-only care. Nest attentiveness and the degree of male contribution to incubation in species with shared incubation were very strongly correlated, whereas this correlation was absent in females. Interestingly, female contribution decreased towards the equator while male contribution did not change significantly with latitude. Hence, relative male incubation effort increased towards the equator, whereas that of female decreased. In species with incubation feeding, female nest attentiveness increased with the frequency of male feeding.
These findings support the hypothesis that male help is indispensable for increasing nest attentiveness in birds, either in the form of incubation feeding (supply of energy) or direct incubation of eggs. We conclude that energy acquisition constraints might be a potent force driving sex-specific contribution to parental care.
... Thus, polygynous males may compensate for any effects of their lowered care by increasing their mating success with 1 or more additional females. Polygynous males also may allocate their contribution unequally among females (Smith et al. 1994) or provide less paternal care as certainty of paternity decreases (Adrian et al. 2005). Paternal activities may be shown as a courtship strategy (cotton-top tamarins [Saguinus oedipus -Price 1990]) or may be correlated with group size, with males providing less care in large groups, where helpers are available (common marmosets [Callithrix jacchus- Rothe et al. 1993]). ...
We studied maternal, paternal, and alloparental care in striped mice (Rhabdomys pumilio), which nest and breed communally in the succulent karoo, South Africa. A total of 18 triads, each consisting of 2 adult female littermates and an unfamiliar adult male, were set up under natural weather conditions. We expected that relationships within captive triads that breed communally would be egalitarian, and that all individuals would participate in the rearing of offspring, but we assumed that the degree of caregiving behavior would vary between mothers, fathers, and alloparents, because individuals obtain different fitness benefits. Social interactions in the triads were predominantly amicable and in the majority of triads, both females produced litters in a communal nest. All 3 adults in a triad participated in care of the offspring, with mothers spending 43%, fathers 26%, and alloparents 24% of observations in caregiving activities. Our results indicate that sisters can for
m stable cooperative relationships, but members of a communal nest allocate their caregiving to individual offspring according to potential trade-offs between direct and indirect fitness benefits. Large amounts of paternal care can occur in a polygynous species, which contrasts with the common belief that paternal care is a characteristic of monogamy.
... Its living members were traditionally arranged in the subfamilies Dolichotinae and Caviinae (Wilson & Reeder, 1993) but today this also includes the subfamily Hydrochoerinae (Woods & Kilpatrick, 2005). The caviines have recently received attention concerning their taxonomy, ecology, palaeontology, behaviour and evolution (Rood, 1970(Rood, , 1972Mones & Castiglioni, 1979;Marquet et al., 1993;Quintana, 1996Quintana, , 1998Quintana, , 2001Ubilla, Piñeiro & Quintana, 1999;Ebensperger & Cofré, 2001;Tognelli, Campos & Ojeda, 2001;Ubilla & Rinderknecht, 2001;Solmsdorff et al., 2004;Adrian et al., 2005;Schilling & Petrovich, 2006;Weisbecker & Schmid, 2007, and references therein). ...
A comparative study of the appendicular skeletal morphology, with a particular emphasis on the autopodial elements (manus and pes), of the extinct caviine rodent Microcavia criolloensis (Late Pleistocene, Uruguay), together with that of living species of Microcavia and some allied caviines is performed. Burrow-digging and above-ground behaviour by M. criolloensis could have evolved in the Late Pleistocene, as with its relative M. australis in the Recent. This is suggested based on the morphology of preserved articulated skeletons along with fossil burrow-like structures. The most remarkable features are: in its forelimb, where the humerus has a structure that would have allowed it to perform similar activities to M. australis, based on humeral width across the epicondiles relative to total humerus length index and a good resistance as indicated by high values relating the diameter of the diaphysis to its total length. Qualitative comparison shows that M. criolloensis had a stout, wide manus with relatively short digits including short, wide phalanges, despite its large size. In its hind limb there is a stout hind-foot with relatively short and wide metatarsals and phalanges, as compared with those of the recent species, that could arguably be considered a useful tool for shovelling out displaced soil. The generalized morphology suggests above-ground behaviour together with digging ability. The environmental adaptations of M. criolloensis are also briefly discussed, which seem to differ from those of its extant relatives. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154, 795–806.
... Overall, biparental care in fishes is more common in species with less intense sexual selection, a relationship that also been suggested for other taxa. In mammals, pair-bonding, sexual selection and sperm competition risk also relate to the evolution of care, with monogamous species showing increased male care (guinea pigs, Galea & Cavia sp., Adrian et al. 2005; mice, Mus sp., Patris & Baudoin 2000). In birds, it appears that sperm competition and intensity of sexual selection are selective pressures on male parental care, and male care increases along with male paternity certainty (Møller 2000;Møller & Cuervo 2000). ...
One of the common assumptions in the study of the evolution of parental care is that trade-offs exist between parental investment and other fitness-related traits. In general, this body of work follows the traditional definition that parental investment (in the current offspring) decreases that individual’s ability to invest in future reproduction (Trivers 1972). However, examination of the empirical evidence shows that assuming a trade-off between parental and mating effort is not always appropriate. This overemphasis on a trade-off between mating and parental effort has arisen in part because of an oversimplification of female reproductive strategies, a failure to consider interactions between the sexes, and a tendency to consider behaviours as unifunctional, thereby ignoring the more complex relationship between mating and parental effort in many species. Here, we first examine the empirical evidence for trade-offs between mating and parental effort in males and females to ask when trade-offs occur and what pattern they take. By highlighting a number of exemplar species, we then explore how the presence or absence of trade-offs relates to mate choice and sexual selection in both sexes. Finally, we highlight the importance of considering individual variation, which has been particularly overlooked in examinations of female investment, and how preferences in one sex may influence the existence and our interpretation of apparent trade-offs in the other sex.
... Asher, unpublished data). Males have extremely large testes, lower body weights than females, are highly compatible, and females have a strong tendency for mating with multiple males (Schwarz-Weig and Sachser 1996;Keil and Sachser 1998;Sachser 1998;Keil et al. 1999;Sachser et al. 1999;Cooper et al. 2000;Hohoff et al. 2003, Adrian et al. 2005. ...
Ecological factors differently affect male and female animals and thereby importantly influence their life history and reproductive
strategies. Caviomorph rodents are found in a wide range of habitats in South America and different social and mating systems
have evolved in closely related species. This permits to study the impact of ecological factors on social evolution. In this
study, we investigated the social organization and the mating system of the wild cavy (Cavia aperea), the ancestor of the domestic guinea pig, in its natural habitat in Uruguay. Based on our laboratory investigations, we
expected a polygynous system with large males controlling access to females. Results from radiotelemetry and direct observations
showed that females occupied small stable home ranges which were largely overlapped by that of one large male, resulting in
a social organization of small harems. In some cases, small satellite males were associated with harems and intermediate-sized
roaming males were occasionally observed on the study site. However, microsatellite analyses revealed that offspring were
exclusively sired by large males of the same or neighboring harems, with a moderate degree of multiple paternity (13–27%).
Thus, the mating system of C. aperea can be described as polygynous and contrasts with the promiscuous organization described for other species of cavies (Cavia magna, Galea musteloides and Microcavia australis) living under different ecological conditions. Our findings stress the strong impact of environmental factors on social evolution
in Caviomorphs as resource distribution determines female space use and, thereby, the ability of males to monopolize females.
... The sex differences observed in defence may be influenced by differences in perceived paternity/maternity certainty and alternative reproductive opportunities. In a wide variety of species, uncertainty in paternity decreases the amount of paternal care provided (birds: Møller & Birkhead 1993;Sheldon & Ellegren 1998;Westneat & Stewart 2003;mammals: Busse 1985;Buchan et al. 2003;Wolff & Macdonald 2004;Adrian et al. 2005;fishes: Neff & Gross 2001;Neff 2003;Rios Cardenas & Webster 2005). A previous field study reported that 41.7% of N. pulcher breeding males did not father all young in their groups; 8 of 35 young could be attributed to extrapair fathers (Hensel 2005). ...
In cooperatively breeding species, members of social groups will risk serious injury or even their lives by actively codefending the communal territory and young in the territory. However, individuals within the group vary in the intensity and frequency of defence. To date little is known about how sex, body size and social status interact with the degree of threat to influence defence activities. To this end, we experimentally manipulated the need for defence in wild groups of the cooperatively breeding cichlid, Neolamprologus pulcher by exposing social groups to four intruder types representing different forms of threat. Intruders were introduced singly (experiment 1) to assess the costs and benefits associated with defence and in tandem (experiment 2) to assess how individuals prioritize perceived threats. Dominant breeders defended more than subordinate helpers, females were more aggressive than males, and female breeders defended more than any other individual in the group. Individual body size, or the difference in body size between intruders and defenders, had no influence on the frequency of defence. Dominant male breeders defended most vigorously against threats to their dominance position, while dominant female breeders showed the highest defence rates to both threats to their position and the security of young to a similar degree relative to all others. Predators evoked the strongest defence responses by subordinate helpers, and conspecific intruders evoked the weakest responses relative to all other intruder types. The results suggest that both costs and benefits have shaped aggressive defence patterns in this cooperatively breeding teleost fish.
... In monogamous species, it is common for established pairs to aggressively defend territories and for males to contribute to the care of the young (Clutton-Brock, 1989;Kleiman, 1977). In G. monasteriensis, adults are highly aggressive with other adults (Hohoff et al., 2002), and males engage in more paternal behavior than in other cavy species (Adrian, Brockmann, Hohoff, & Sachser, 2005). To date, behavioral interactions of the young with the mother or other adult females in G. monasteriensis have not been described. ...
The authors compared interactions of infants with mothers and unfamiliar females in a novel environment in 2 caviomorph rodent species: the harem-living Cavia aperea, the probable progenitor of the domestic guinea pig; and the pair-living Galea monasteriensis. In C. aperea, interactions with mothers and unfamiliar females were largely similar; in G. monasteriensis, interactions with the mother, but not unfamiliar female, were characterized by physical closeness and sociopositive behavior. In G. monasteriensis, plasma cortisol levels were lower when with the mother than when with the unfamiliar female. Results are consistent with the species' social organizations and suggest that behavioral interactions of pups with mothers and other females in domestic guinea pigs reflect primarily the social organization of the progenitor species rather than domestication.
... playing and grooming) has been reported in mammalian species with a high certainty of paternity. For example, paternal care has been demonstrated in wild guinea pigs (Cavia aperea) who exhibit a polygynous mating system compared to the yellow-toothed guinea pig (Galea musteloides) which mates promiscuously (low paternity certainty) and therefore shows no paternal care (Adrian et al., 2005). ...
One of the most important assumptions of kin selection theory is that individuals behave differently towards kin than non-kin. In mammals, there is strong evidence that maternal kin are distinguished from non-kin via familiarity. However, little is known about whether or not mammals can also recognize paternal kin as many female mammals, including primates, mate with multiple males near the time of conception, potentially concealing paternal kinship. Genetic data in several mammalian species with a promiscuous mating system and male-biased dispersal reveal a high skew in male reproduction which leads to co-residing paternal half-siblings. In most primates, individuals also form stable bisexual groups creating opportunities for males to interact with their offspring. Here I consider close paternal kin co-resident in the same social group, such as father-offspring and paternal half-siblings (i.e. animals sharing the same father but who were born to different mothers) and review mammalian studies of paternal kin discrimination. Furthermore, I summarize the most likely mechanisms of paternal kin discrimination (familiarity and phenotype matching). When familiarity is the underlying mechanism, mothers and/or the sire could mediate familiarity among paternal half-siblings as well as between fathers and offspring assuming mothers and/or fathers can assess paternity. When animals use phenotype matching, they might use their fathers' template (when the father is present) or self (when the father is absent) to assess paternal kinship in others. Available evidence suggests that familiarity and phenotype matching might be used for paternal kin discrimination and that both mechanisms might apply to a wide range of social mammals characterized by a high skew in male reproduction and co-residence of paternal kin. Among primates, suggested evidence for phenotype matching can often have an alternative explanation, which emphasizes the crucial importance of controlling for familiarity as a potential confounding variable. However, the mechanism/s used to identify paternal kin might differ within a species (as a function of each individual's specific circumstances) as well as among species (depending upon the key sensory modalities of the species considered). Finally, I discuss the possible cues used in paternal kin discrimination and offer suggestions for future studies.
Understanding the morphotypical masculinization gradient and its impact on social behavior in a natural animal model is essential for unraveling sexual differentiation dynamics and their ecological implications. In this study, we examined the presence of a morphotypical masculinization gradient in female wild cavies (Cavia aperea) and its association with social behavior. Experimental colonies in four enclosures with different initial population densities were established. Between October 2017 and June 2018, we collected two datasets. The first dataset included body mass and anogenital distance (AGD) from 48 females, collected every 15–30 days. Simultaneously, focal behavioral observations were carried out during the intervals between recaptures. The behavioral dataset encompassed 65 marked cavies (males and females); 50 in high-density and 15 low-density conditions. Behavioral data were utilized to construct a focal association index matrix. Social centrality by spatial proximity measures were calculated using eigenvector analysis. Using the AGDI as a proxy for masculinization, we categorized females into three groups based on their AGDI values: low, middle, and high. The AGDI demonstrated high repeatability, underscoring its stability as a metric. Morphotype analysis revealed distinct distributions of AGDI values across varying initial density conditions. No significant associations were found between AGDI values and social centrality. These findings enhance our understanding of social dynamics in C. aperea and emphasize the significance of accounting for morphotypical variability in ecological research.
What really differentiates us from our relatives in the animal world? And what can they teach us about ourselves? Taking these questions as his starting point, Norbert Sachser presents fascinating insights into the inner lives of animals, revealing what we now know about their thoughts, feelings and behaviour. By turns surprising, humourous and thought-provoking, Much Like Us invites us on a journey around the animal kingdom, explaining along the way how dogs demonstrate empathy, why chimpanzees wage war and how crows and ravens craft tools to catch food. Sachser brings the science to life with examples and anecdotes drawn from his own research, illuminating the vast strides in understanding that have been made over the last 30 years. He ultimately invites us to challenge our own preconceptions – the closer we look, the more we see the humanity in our fellow creatures.
To investigate the utility of ramps as enrichment and as a method for establishing demand for commodities, the latency to climb a ramp of increasing slope to obtain food was measured in four guinea pigs. The average height where guinea pigs failed to climb was 29.1 cm (slope 14.2 degrees). In addition, the increasing slope altered climbing behavior; when climbing speed was tested using the same slope for all trials within a single session, the guinea pigs maintained their climbing speed as the gradient increased across sessions. In comparison, when the slope was increased with each successful climb within a session, climbing speed was not maintained. Installing the maximum slope climbed can promote increased exercise and foraging but avoid physical harm or barriers to resources. Furthermore, these results indicate that climbing, a simple behavior with measurable differences as a function of slope and thus, effort, could be used as a method for testing the demand for commodities, such as food type or enrichment items, to be included in the husbandry of guinea pigs to improve welfare of the small cavy.
Mating system theory based on economics of resource defense has been applied to describe social system diversity across taxa. Such models are generally successful but fail to account for stable mating systems across different environments or shifts in mating system without a change in ecological conditions. We propose an alternative approach to resource defense theory based on frequency-dependent competition among genetically determined alternative behavioral strategies characterizing many social systems (polygyny, monogamy, sneak). We modeled payoffs for competition, neighborhood choice, and paternal care to determine evolutionary transitions among mating systems. Our model predicts four stable outcomes driven by the balance between cooperative and agonistic behaviors: promiscuity (two or three strategies), polygyny, and monogamy. Phylogenetic analysis of 288 rodent species supports assumptions of our model and is consistent with patterns of evolutionarily stable states and mating system transitions. Support for model assumptions include that monogamy and polygyny evolve from promiscuity and that paternal care and monogamy are coadapted in rodents. As predicted by our model, monogamy and polygyny occur in sister taxa among rodents more often than by chance. Transitions to monogamy also favor higher speciation rates in subsequent lineages, relative to polygynous sister lineages. Taken together, our results suggest that genetically based neighborhood choice behavior and paternal care can drive transitions in mating system evolution. While our genic mating system theory could complement resource-based theory, it can explain mating system transitions regardless of resource distribution and provides alternative explanations, such as evolutionary inertia, when resource ecology and mating systems do not match.
In most mammalian species, females regularly interact with kin, which is expected to reduce aggressive competitive behaviour among females. It may thus be difficult to understand why infanticide by females has been reported in numerous species and is sometimes perpetrated by groupmates. Here, we investigate the evolutionary determinants of infanticide by females by combining a quantitative analysis of the taxonomic distribution of infanticide with a qualitative synthesis of the circumstances of infanticidal attacks in published reports. Our results show that female infanticide is widespread across mammals and varies in relation to social organization and life history, being more frequent where females breed in groups and have intense bouts of high reproductive output. Specifically, female infanticide occurs where the proximity of conspecific offspring directly threatens the killer's reproductive success by limiting access to critical resources for her dependent progeny, including food, shelters, care or a social position. By contrast, infanticide is not immediately modulated by the degree of kinship among females, and females occasionally sacrifice closely related infants. Our findings suggest that the potential direct fitness rewards of gaining access to reproductive resources have a stronger influence on the expression of female aggression than the indirect fitness costs of competing against kin.
This article is part of the theme issue ‘The evolution of female-biased kinship in humans and other mammals’.
In most mammalian species, females regularly interact with kin, and it may thus be difficult to understand the evolution of some aggressive and harmful competitive behaviour among females, such as infanticide. Here, we investigate the evolutionary determinants of infanticide by females by combining a quantitative analysis of the taxonomic distribution of infanticide with a qualitative synthesis of the circumstances of infanticidal attacks in published reports. Our results show that female infanticide is widespread across mammals and varies in relation to social organization and life-history, being more frequent where females breed in group and invest much energy into reproduction. Specifically, female infanticide occurs where the proximity of conspecific offspring directly threatens the killer's reproductive success by limiting access to critical resources for her dependent progeny, including food, shelters, care or a social position. In contrast, infanticide is not immediately modulated by the degree of kinship among females, and females occasionally sacrifice related juveniles. Our findings suggest that the potential direct fitness rewards of gaining access to reproductive resources have a stronger influence on the expression of female aggression than the indirect fitness costs of competing against kin.
We took the rare opportunity to observe and quantify spontaneous allosuckling in a captive group of Cavia aperea captured in the wild (a male, two females and their offspring). We recorded behavior interactions between all offspring and each of the adults between days 6 and 20 of life. Infants suckled equally from their mother and from the other female, which differs from a previous report in which mothers typically nursed own young. In addition, infants stayed closer to the other female than to mother or to the father. We discuss these results in the light of the common occurrence of allosuckling in Cavioidea and social structure.
Relative investment in reproduction is a major factor in the evolution of mating systems in mammals: since females invest so much more (gestation + lactation) than males, the most common mating system in this group is polygyny. Ecology, mainly in the way it promotes aggregation among females, modulates this main pattern. This chapter reviews the mating systems of caviomorphs (including an assessment of sexual selection and sperm competition where relevant) within this framework. It also attempts to unravel the relative roles of present ecology and phylogeny in the currently observed mating systems. It finds that monogamy is––as expected––the least frequent of mating systems among caviomorphs, found only in maras, pacas (probably) and one species of cavy. In the case of maras, ecology is clearly crucial, as resource scarcity and dispersion force the male to follow one female everywhere she goes, leading to monogamy. Among the social caviomorphs, again as expected, polygyny is the most common pattern for capybaras, coypus, several cavies, the group-living burrowing species of Ctenomyidae and possibly Octodontidae. A few species are clearly promiscuous (both males and females) leading to sperm competition and consequently large testes, as in the cavy Galea musteloides. The chapter also reviews instances of intra-specific variation in the mating system (and the social system) as in capybaras which appear to form pairs in the forest while their most common situation is the social and mainly polygynous groups of the savannas. In contrast, maras remain monogamous even when fed ad libitum in captivity. Several avenues for further research are discussed, such as a comparison of burrowing caviomorphs and the study of scent glands as sexually selected traits. This review shows how caviomorphs exhibit the whole range of mating systems described for mammals and how they can contribute to our understanding of their evolutionary origin and maintenance.
Understanding the fitness consequences of group-living and breeding strategies is critical to advancing a theory for the evolutionary significance of animal social systems. To date, our understanding of the fitness consequences in caviomorphs is limited to six species. The available evidence suggests that sociality positively affects fitness in female capybaras and increases offspring survival in maras. Laboratory studies suggest that the number of males or the dominance status of females is an important predictor of female reproductive success in two cavies. In colonial tuco-tucos, per capita direct fitness is lower in groups than for solitary females, suggesting an immediate cost to sociality. In degus, the fitness consequences of sociality depend on the time frame of study. In studies encompassing two or three years, the direct fitness of degu females decreases with increasing group size. However, a recent study encompassing eight years revealed that the relationship between direct fitness and group size is most positive in years with low mean rainfall and food abundance, suggesting that sociality has evolved as a means to ensure reproductive success under harsh conditions. To advance our understanding, it is critical that researchers quantify fitness consequences of group-living in more species. In well-studied species, researchers have the opportunity to determine the extent of intra-specific variation in sociality–fitness relationships as well as use modern analytical tools to quantify how social interactions within groups influence individual reproductive success and reproductive skew.
Caviomorphs occupy diverse ecological niches and exhibit diverse social organization. Studies and theory derived from better-studied mammalian taxa establish an integrative and comparative framework from which to examine social systems in caviomorphs. We synthesize the literature to evaluate variation in space use, group size, mating systems, and parental care strategies in caviomorphs in the context of current hypotheses. Across species, ecological lifestyles, including diet, habitat mode, space use, and activity period, are linked to variation in social systems including mating systems, breeding strategies, and associated parental care strategies. Within species, different populations and the same populations over time vary in space use, sociality, and mating systems, with most variation explained by differences in resource distribution, predation risk, or population density. We highlight unique aspects of caviomorph biology and offer potentially fruitful lines for future research both at the inter- and intra-specific levels. Among species, better-resolved phylogenies and collation of basic natural history information, including lifestyle characteristics, especially for underrepresented families such as spiny rats (Echimyidae) and porcupines (Erethizontidae), can advance comparative studies. Within species, future studies of caviomorphs can make use of recent technological advancements in data collection (e.g. proximity data loggers) and data analysis (e.g. model selection), as well as integration of laboratory and field studies. These complementary approaches will allow us to examine the diversity of social behavior in this rich taxon at multiple levels of analysis. In doing so, we can gain unique insights into the ecological drivers and evolutionary significance of diverse social systems.
This chapter discusses the facility design, environment, and basic husbandry recommendations for the guinea pig. Although general laboratory animal facility design and principles for rats, mice, and hamsters have applicability to the guinea pig, characteristics and behavior unique to this species have fostered implementation of new and/or adjunct husbandry practices to improve the care and use of this laboratory animal. In addition to the natural behavior and physiology of the species, the nature of the research activity performed considers planning, design, or modifications of guinea pig holding rooms. Quarantine facilities, breeding colonies, conventional and infectious disease research have different requirements for housing. The Guinea pigs are generally docile and seldom bite; however, they are easily frightened and will try to avoid capture or being held. This chapter further explains the housing condition required for guinea pigs, which includes the right ventilation, illumination, temperature, humidity, sanitation, noise conditions, and space requirements. Ventilation for laboratory animals should balance air quality, animal comfort, and energy efficiency to provide cage environments that will optimize animal welfare and research results. Furthermore, the chapter reviews the nutritional diseases and record keeping of guinea pigs. For the identification of the animals, cage cards are used and the cards should include the strain of guinea pigs, sex, number, principal investigator, and research protocol identification.
Male mammals often kill conspecific offspring. The benefits of such infanticide to males, and its costs to females, probably
vary across mammalian social and mating systems. We used comparative analyses to show that infanticide primarily evolves in
social mammals in which reproduction is monopolized by a minority of males. It has not promoted social counterstrategies such
as female gregariousness, pair living, or changes in group size and sex ratio, but is successfully prevented by female sexual
promiscuity, a paternity dilution strategy. These findings indicate that infanticide is a consequence, rather than a cause,
of contrasts in mammalian social systems affecting the intensity of sexual conflict.
When separated from their mother and other group members, guinea pig Cavia porcellus pups emit distinctive high pitched whistles. To determine if these vocalisations are individually distinctive, we recorded the whistles of isolated guinea pig pups, 8 to 10 days old, and subjected their acoustical parameters to discriminant analysis. The results of the reclassification accuracy were higher than random assignment, indicating the existence of individual differences. Individual pup vocalisations did not differ from one another by any single acoustic parameter, but by a set of parameters. Individual recognition of such isolation calls by mothers could play an important role in facilitating reestablishment of contact.
Parental care is a widely spread phenomenon in the animal kingdom. Parental investment in offspring is the result of a trade-off between two opposite trends. On the one side, parental care does increase the offspring’s chance of surviving, on the other side, it pospones the parent’s return to reproduction. The resulting trade-off varies according to several factors and can generate conflicts between the parents and between the parents and their offspring. Parental care does not necessarily imply the existence of a differentiated parent/offspring bond. When a such a bond exists, the form it takes and its durability varie across species, as well as its consequences - often great - on offspring’s life. We do not aim at being thorough – it would be impossible within the lenght of an article – but at presenting the main actual concepts and their connections by examples drawn from various species.
Cavies (family Caviidae) are a group of rodents distributed over much of South America. The high diversity of habitats inhabited by different species is paralleled by a high diversity of social organizations. Comparisons of behavioral and reproductive strategies between species can provide valuable insights into mammalian social evolution. In this review we 1st summarize the literature to give an idea of the diversity of social and mating systems within the genera Cavia, Galea, Microcavia, and Kerodon. Social systems range from solitary animals through pairs and harems to multimale–multifemale groups. Mating systems of cavies include monogamy and promiscuity and different forms of polygyny. We then review behavioral strategies of females and males that account for this social diversity. Particularly, the role of females and the potential of males to monopolize mates are examined. In some species, for example, estrous females actively solicit copulations with several males and thereby prevent their monopolization by single males. We also discuss adaptations of reproductive physiology to different mating systems. Finally, environmental factors influencing aspects of the social and mating systems of cavies are considered. Particularly, differences in resource distribution, predation risk, and climatic conditions might explain the great variation in species social organization.
Patterns of mate choice may be important determinants of a species’ social organisation and mating system. At least two different aspects of female mate choice can be distinguished: choice of a social partner and choice of the genetic father of the offspring. Different characteristics of males can qualify them for these two roles. Although social and reproductive partners have been shown to differ in many species, social association times are often used in laboratory choice tests to infer reproductive preferences. The traits for which females may choose partners are diverse. Body size can correlate with the male’s strength in defending resources or other abilities benefiting the female and her offspring. In species living in social groups, social skills learned from group members during infancy can be important for later reproductive success. In this laboratory study, we conducted choice tests with wild cavies, Cavia aperea, a harem-living species of South American rodents, to determine social preferences of females towards two simultaneously available males. For offspring sired during these tests, paternities were determined by microsatellite DNA profiling. Males used in the tests differed in body weight and in rearing conditions: Half of the males had been reared in the presence or absence of their father, respectively. Male rearing conditions had no effect on either female social preferences or paternities. Females significantly preferred heavier males as social partners. In five of six tests, the heavier male also sired the offspring. Sires were in most cases but not consistently socially preferred. Heavier males may be preferable as social partners because they are better able to provide females with resources or have more experience in paternal care or predator avoidance as weight correlates with age. When choosing reproductive partners, females may prefer other male traits and the distribution of paternities may also be influenced by sperm competition.
In many species parental care is needed to rear offspring that survive to reproduce, a good measure of benefits in fitness
terms. Such care may involve major costs to the individual. Balancing benefits and costs of care almost inevitably leads to
tensions among individuals that provide and use the resource ‘parental care’. Thus parental care and with it parental investment
(i.e. the ultimate costs of care) is enacted in a game of conflict and cooperation. Using mostly examples from mammals, I
discuss Tinbergen’s four questions as they apply to parental care. Phylogenetic analyses of parental care are complicated
by substantial intraspecific variability of this trait. Understanding the physiological and ontogenetic processes underlying
parental care behaviour helps to understand how differences in the cost of care depend on the state of parents and their environment.
A deeper insight into the strategies of conflict and cooperation in care can be derived from consideration of the behavioural
mechanisms available to participants.
A combination of field and laboratory investigations has revealed that the temporal patterns of testosterone (T) levels in blood can vary markedly among populations and individuals, and even within individuals from one year to the next. Although T is known to regulate reproductive behavior (both sexual and aggressive) and thus could be expected to correlate with mating systems, it is clear that the absolute levels of T in blood are not always indicative of reproductive state. Rather, the pattern and amplitude of change in T levels are far more useful in making predictions about the hormonal basis of mating systems and breeding strategies. In these contexts we present a model that compares the amplitude of change in T level with the degree of parental care shown by individual males. On the basis of data collected from male birds breeding in natural or captive conditions, polygynous males appear less responsive to social environmental cues than are monogamous males. This model indicates that there may be widely different hormonal responses to male-male and male-female interactions and presumably equally plastic neural mechanisms for the transduction of these signals into endocrine secretions. Furthermore, evidence from other vertebrate taxa suggests strongly that the model is applicable to other classes
This study aims to elucidate the social system of the wild cavy (Cavia aperea), the feral ancestor of the domestic guinea pig, whose behavior under natural conditions is almost unstudied. Therefore, a population of C. aperea was investigated for a 6-month period in its natural habitat in southeastern Brazil. The animals' space use was examined via radiotelemetry, social interactions were recorded using direct observations, and genetic relationships were analyzed via DNA fingerprinting. Additionally, the distribution of plant cover, food resources, and predation risk was recorded to investigate the impact of different ecological factors on evolution of the social system. In the study period, a low population density was detected and a strong predation pressure existed, which resulted in a high mortality rate of C. aperea. Spatial distribution of wild cavies was strongly associated with areas of dense ground vegetation. Within these areas, small groups consisting of 1 male and 1-2 females occupied stable home ranges that overlapped only slightly with home ranges of adjacent groups. Social interactions were restricted mainly to individuals of the same group, and initial analyses of paternity indicate that the females' offspring were sired by the respective group male. The social system and spatial organization of C. aperea are regarded as adaptations to high predation pressure because in dense vegetation small group size reduces the risk of detection by predators. Moreover, habitat use, social interactions, and paternity point to a single-male system in this low-density population of wild cavies.
Avian species differ markedly in the extent to which males contribute to pre-hatching and posthatching parental care. In a recent comparatives study, Moller and Birkhead (1993) concluded that diversity in male parental care was associated with differences among species in extrapair paternity. Specifically, their results showed a significant inverse relationship between extrapair paternity and male contributions to feeding of nestlings. We used a revised and updated data set in an attempt to replicate their study. In contrast to their results, we found no evidence that the evolution of male posthatching care was strongly correlated with paternity. Instead, our results showed that male participation in incubation tends to be negatively associated with extrapair fertilization rates, thereby providing tentative support for Ketterson and Nolan's (1994) hypothesis that this particular form of parental care may be especially restrictive to male extrapair mating activities.
Aggression and paternal behavior can be linked in a variety of ways, and the relationship between hormones and these social behaviors may be equally variable. We have illustrated how high levels of aggression can be compatible with high levels of paternal care. Under such conditions, T may be positively associated with paternal care and aggression, even in species in which a decrease in T occurs with the onset of paternal care. Similar to T, AVP also can be positively associated with both aggression and paternal care. Individual variation in paternal care and aggression may be mediated by variation in AVP and T levels and receptors. This physiological variation could in turn be important for survival of offspring and also for shaping variation in paternal behavior and aggression of those offspring. Behavioral and endocrine changes may be passed on to multiple generations. The degree of plasticity in these relationships remains to be elucidated, but our results suggest that variation in AVP and T may be important for altering paternal and aggressive behaviors in response to the social environment.
Reproductive effort, defined as the cost in energy spent and risks taken in reproduction, has two components: parental effort and mating effort. Environmental uncertainties influencing juvenile survivorship affect the temporal pattern of parental effort: when the parent cannot decrease offspring mortality by increased investment, it must minimize the effort invested in offspring which die. Environmental uncertainty responsible for juvenile mortalities before the termination of parental care causes juveniles to have low reproductive values and is responsible for the apparently widespread tendency toward low early parental effort. Several predictions about the pattern of expenditure of parental effort result, although at present the empirical bases for testing these predictions fully are inadequate, and comparisons are largely inferential. A comparison of marsupial and placental parental strategies as a test of these predictions suggests that marsupials have long been under selection imposed by frequent los...
Male parental care is rare in most groups of animals but common in birds. Among birds considerable variation exists in the form of care provided their young; recent developments in several areas may help to explain this variation. These include (i) improvements in the comparative method, particularly the use of phylogenies to investigate questions about the evolution (origin) of behavior; (ii) field studies designed to determine the fitness benefits of care and the selective factors that maintain it; and (iii) investigations of the mechanisms of care, especially its neural and hormonal bases. The greatest challenge to functional explanations of male care has come from the revelation that males frequently provide care for offspring that are not genetically their own. Resolving this apparent paradox will require more accurate accounting of the costs and the benefits of care, and greater attention to the form of care provided by males. Data support the following working hypothesis: In taxa in which males incubate, as opposed to providing other forms of care, sexual selection may be less intense and males may resemble females more in appearance and physiology. Males may also be more likely to be the genetic sires of the offspring they care for, perhaps because of the greater cost to females of multiple matings or perhaps because male incubation is incompatible with sustained sexual behavior. Ultimately, an integrated consideration of history, function, mechanism, and development should reveal the interplay of factors that have led to male parental care in birds and that account for its maintenance in various forms today.
Parental behavior and pup development in meadow and prairie voles were examined. Social units were manipulated for the presence of fathers and of juveniles. Meadow vole mothers alone with pups showed less maternal care and spent more time resting than did mothers with juveniles or with fathers and juveniles. Pups reared only with mothers developed faster than did pups under other conditions. Number of animals in the social unit was negatively correlated with the rate of pup development. Meadow vole fathers and juveniles showed no parental care. In contrast, prairie vole mothers spent less time in the nest when both fathers and juveniles were present. Fathers assisted in rearing pups, and litters developed more rapidly when fathers were present. Juveniles remained in the natal nest and engaged in parentlike behavior. The findings relate to differences in the life history strategy for the 2 vole species. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Parental behaviour was directly observed during two 30-min bouts on each of the first 18 days after birth for both Djungarian, P. campbelli, and Siberian, P. sungorus, dwarf hamster litters. Results were consistent with predictions based on earlier studies that demonstrated a positive impact of paternal presence on pup survival in P. campbelli, but not P. sungorus. The presence of the father or an aunt significantly decreased, by about half, the proportion of time that pups were alone in P. campbelli. Because brief parental absences were unlikely to result in pup cooling, analyses also considered only those absences that were 3 min or longer. By those criteria, P. campbelli pups housed with a second adult were rarely alone. In contrast, the father had little impact on the parental care received by pups in P. sungorus. Phodopus sungorus males were rarely alone in the nest with the pups, whereas both fathers and aunts in P. campbelli were alone with the pups significantly more often than the mother from mid-lactation until weaning. This behaviour reflected temporal coordination between the behaviour of the adults. Pups were left alone less often than expected based on the independent behaviour of each adult. Because there was no reason to expect alloparental care by aunts in the wild, the presence of a second adult, rather than specific parental behaviour by that adult, may be the essential component of increased pup survival. Limited observations of male parental care in the wild demonstrated that significant paternal care could occur in P. campbelli. Both field and laboratory data, however, suggest that biparental care would be facultative and adaptive under certain environmental conditions (e.g. extreme temperatures) but not all.
Adult male Mongolian gerbils, Meriones unguiculatus, avoid contact with their young on the day that the young are born. However, on succeeding days, fathers spend nearly as much time in contact with their offspring as do mothers. We undertook a series of studies to investigate the causes of the day-to-day change in male parental behaviour. In experiment 1, we tested males' response to pups before, after and on the day of their mates' parturition, and found that males were more parental both before and after the day of birth of their young than on that day. In experiment 2, we compared the parental behaviour of males paired either with intact or with ovariectomized dams (which do not come into postpartum oestrus) and found that males that were mated to intact females were less attentive to pups on the day of their birth than were the males mated to ovariectomized females. In experiment 3, we compared the parental responses of castrated and intact males to newborn pups and found that castrated males were more parental than intact males. In experiment 4, we compared the parental responses of males that were exposed to postpartum oestrous females but prevented from mating for 24 h. Extending the period of male sexual arousal to 24 h inhibited paternal responsiveness to neonates for 24 h. We interpret these results as being consistent with the hypothesis that on the day of birth of a litter, a male's parental behaviour is inhibited by the motivation to mate during his partner's postpartum oestrus.
In a laboratory experiment, we investigated paternity in the regularly multiple-mating yellow-toothed cavy (Galea musteloides) using multilocus DNA fingerprinting. In three mixed-sex groups (four males and six to seven females), multiple paternity was found in 15 of 18 litters. In all groups, males organized themselves in linear dominance hierarchies. Males of all ranks sired offspring, but higher ranking males achieved significantly greater reproductive success than lower ranking males.
Based on the model of Whittingham et al. (1992, Am. Nat., 139, 1115-1125), it is predicted that males in many monogamous species of birds will not decrease their level of parental care until their confidence of paternity is very low (threshold response). This prediction was tested by holding monogamous male tree swallows, Tachycineta bicolor, in captivity for 1 or 3 days during their mate's fertile (pre-laying, laying) or non-fertile (incubation) periods. Males were held in cages with one-way glass that allowed them to see their mates engage in extra-pair copulations. Females increased their rate of extra-pair copulation when their mates where held in captivity during pre-laying and laying. Therefore, the confidence of paternity of these captive males was lower than unmanipulated males or males held during incubation (controls). Although the male's access to his fertile mate was reduced by up to 57%, there was no effect of the timing or length of captivity on the male's share of feeding nestlings or his defence of the nest. Male tree swallows did not reduce their parental effort over a wide range of paternity, and previous studies showed they commit infanticide when their paternity is zero, suggesting that they exhibit a threshold response to decreasing paternity. Furthermore, a review of several studies suggests that other monogamous species also exhibit a threshold response to decreasing paternity.
Parentage is the proportion of juveniles in a brood that are offspring of potential care givers. We analyzed how reductions in parentage affect the evolution of parental behavior using a static optimization model. The main benefit of parental effort was an increase in the survival of offspring, and the main costs were reduced opportunities to seek additional matings or to parasitize neighbors and/or reduced survival. Both the costs and benefits included terms for relatedness to young. The effect of parentage depended on (1) whether parents responded in ecological time (facultative response) or in evolutionary time (nonfacultative response), (2) whether the cues enabling assessment of parentage permitted discrimination among off- spring, and (3) whether parentage was the same among different groups of juveniles (unrestricted) or varied between them (restricted). When parents did not know their own parentage and mean parentage was the same for all matings, reduced parentage affected the costs and benefits equally, so, as in several previous models, there was no effect on the optimal level of parental effort. Parentage did affect optimal parental effort when mean parentage to the present brood differed from that to young from alternative or future matings. Lowered parentage reduced optimal parental effort when the cost of parenting was missed opportunities for extrapair copulations or brood parasitism or when parentage was consistently higher in alternative or future matings. Nonlinear changes in parentage with age gave complex trajectories of parental care, with individuals of different ages having similar parentage but exhibiting different levels of parental effort. Correlations between parentage and other variables in the model (such as opportunities for additional matings) sometimes masked, but never eliminated, the effects of parentage. When parents could discriminate their own young in a brood, overall parental effort was reduced, but nepotism was increased. When parents could not discriminate their own offspring but had general cues about average parentage to the brood, effects varied depending on the costs and benefits of parental behavior. When parental behavior was costly to care givers, parentage had more effect than when parenting was not costly. Likewise, parentage had less effect when care greatly increased offspring survival than when care was less necessary. Our analyses reconcile conflicting results from previous models and suggest a general framework for analyzing parental behavior within populations and among higher taxonomic groups. Key words: paternity, maternity, parental investment, uncertain parentage, relatedness, optimization models, extrapair copulations, intraspecific brood parasitism. (Behav Ecol 4:66-77 (1993))
Traits of parental behaviour by sexual partners of Calomys musculinus and C. laucha were studied in order to understand their specific mating systems. During during postpartum C. laucha increased significantly the size and modified the shape of the nests when compared with its own prepartum record. In constrast, C. musculinus builds nests of the same size and shape at both pre- and postpartum situations. When co-occupancy of the nest was studied, it was found that C. musculinus partners occupied separate nesting chambers during both pre- and postpartum observations; while C. laucha partners occupied separate chambers of the same nest before delivery but moved to the same nesting chamber after delivery. In experiment II, differences in direct parental care among studied species were found for several behavioural categories. The females of both species scored significantly higher than males in nest building, licking-handling, crouching and retrieving pups. This general pattern was maintained by C. musculinus when in a single partner situation, while C. laucha males, increased licking, handling and pup sniffing in the same situation. None of the species displayed an overt paternal behaviour; however, the male C. laucha shared the nest with the dam and showed more interactions with the pups than the C musculinus counterpart. This is consistent with previous observations suggesting that C. laucha, but not C. musculinus, might be a monogamous species.
We present a theoretical framework in order to understand how the relationship between male parental care and paternity is dependent on the relationship between male parental care and offspring recruitment. When there is an S-shaped relationship between offspring recruitment and the parental care of a single male, we predict a threshold relationship between male parental care and paternity. Tree swallows, monogamous dunnocks, and red-winged blackbirds may follow this pattern. Alternatively, when there is a concave-down relationship between offspring recruitment and male parental care. we predict a continuous (gradual) decline in male parental care in response to decreasing paternity. Studies of noisy miners and polyandrous dunnocks suggest this pattern. Our model illustrates that the relationship between male parental care and paternity is more complex than assumed previously. A predicted adjustment of male parental care in response to paternity must be examined in relation to the effect of male parental care on offspring recruitment and the effect of alternative activities on male fitness.
Paternal care in microtines has been studied infrequently and few studies have compared patterns of direct and indirect paternal investment. The paternal behaviour of three vole species, the meadow vole (Microtus pennsylvanicus), the pine vole (M. pinetorum) and the prairie vole (M. ochrogaster) was examined in a semi-natural setting. Prairie and pine voles were found to exhibit high levels of paternal care. Prairie vole males contributed the most direct care by remaining in the natal nest for long periods of time in contact with the pups. Pine voles contributed less direct care than prairie voles as they spent less time in the natal nest with their offspring. In addition, both prairie and pine vole males were observed to groom their pups and retrieve them back to the nest area. Prairie vole males also engaged in such indirect forms of care as nest construction and maintenance, while pine voles provided indirect care in the form of tunnel construction and food caching. Meadow vole males were the least paternal of the three species and rarely engaged in either direct or indirect care. These findings support predictions that M. pennsylvanicus is promiscuous and that male and female meadow voles occupy separate territories. They are also consistent with studies which indicate that prairie and pine voles are monogamous and have a structured social organization with members interacting closely with one another.
A variety of approaches have been used to understand the evolution of male parental care. General frameworks are provided by Trivers’ theory of sexual selection (1972), the theory of life history strategies (see Horn, 1978; Stearns, 1976) and game theory (Grafen and Sibly, 1978; Maynard Smith, 1977). The factors invoked to explain male parental investment have varied with the level of analysis; intrinsic biological factors such as internal versus external fertilization (Dawkins and Carlisle, 1976; Ridley, 1978) or the capacity to invest (Orians, 1969) have been used to illuminate differences between large taxonomic units such as the vertebrate classes; ecological factors such as harshness (Wilson, 1975), richness (Jenni, 1974), and unpredictability (Pitelka et al., 1974) have all been invoked to explain the presence of unusual levels of male investment in smaller taxonomic units.
The neuropeptide oxytocin has been implicated in the mediation of several forms of affiliative behavior including parental care, grooming, and sex behavior. Here we demonstrate that species from the genus Microtus (voles) selected for differences in social affiliation show contrasting patterns of oxytocin receptor expression in brain. By in vitro receptor autoradiography with an iodinated oxytocin analogue, specific binding to brain oxytocin receptors was observed in both the monogamous prairie vole (Microtus ochrogaster) and the polygamous montane vole (Microtus montanus). In the prairie vole, oxytocin receptor density was highest in the prelimbic cortex, bed nucleus of the stria terminalis, nucleus accumbens, midline nuclei of the thalamus, and the lateral aspects of the amygdala. These brain areas showed little binding in the montane vole, in which oxytocin receptors were localized to the lateral septum, ventromedial nucleus of the hypothalamus, and cortical nucleus of the amygdala. Similar differences in brain oxytocin receptor distribution were observed in two additional species, the monogamous pine vole (Microtus pinetorum) and the polygamous meadow vole (Microtus pennsylvanicus). Receptor distributions for two other neurotransmitter systems implicated in the mediation of social behavior, benzodiazepines, and mu-opioids did not show comparable species differences. Furthermore, in the montane vole, which shows little affiliative behavior except during the postpartum period, brain oxytocin receptor distribution changed within 24 hr of parturition, concurrent with the onset of maternal behavior. We suggest that variable expression of the oxytocin receptor in brain may be an important mechanism in evolution of species-typical differences in social bonding and affiliative behavior.
Provides a general framework for analyzing the effects of a relatively large number of variables on quantitative variation in parental care. On the assumption that natural selection favors parents that maximize their reproductive value in each of many time intervals throughout a breeding attempt, the model predicts optimal parental responses to variation in age and number of offspring, time since the beginning of the breeding season, effort of the mate, and parental condition.-from Author
Males should invest in mate attraction, mate guarding and paternal care in relation to the marginal fitness value of each of those behaviours. Since time and energy are limited, trade-offs between these activities are expected. This study demonstrates that monogamous male European starlings (Sturnus vulgaris) decrease their paternal effort in response to increased opportunities to attract additional mates and instead invest in mate attraction. Monogamous males' probabilities of attracting additional females were increased by providing them with additional nestboxes. This resulted in both the rate at which males were visited by prospecting females and the probability that they would obtain secondary mates increasing. Males with an additional nestbox sang more than males with only one nestbox, both before laying and during incubation. Males with two nestboxes spent more time at their nest sites when their fertile females were away before, but not during, egg laying. The experiment affected how much males incubated during the early, but not during the late, part of the incubation period. This makes sense, because males can attract additional females mainly during the early part of the incubation period. Male feeding of nestlings was unaffected by the experiment. The fact that the potential to attract mates affects males' investment in parental care suggests that variation in this potential may contribute to the variation in paternal care between bird species.
Sperm competition has important consequences for the evolution of paternal care, the most obvious of which is that males should be selected not to care for young that they are unlikely to have fathered. This chapter aims to unravel the original approach to the problem, both theoretically and empirically. However, the adaptive adjustments in the level of care by males in response to reduced paternity are considered in the context of the mating system as a whole, including patterns of extra-pair matings. This is because life history decisions regarding paternity and paternal care are closely linked to other components of the mating system, such as the extent of male investment in extra-pair mating with additional females. Thus, using this whole mating system approach, it may be possible to explain the failure of a number of recent empirical studies to demonstrate a reduction in male care following the loss of paternity. Only with a detailed understanding of patterns of extra-pair mating, we can make correct predictions regarding the effect of paternity on paternal care, and especially the existence of facultative vs. nonfacultative responses to a reduced probability of paternity.
We summarize our studies on the social and mating systems of Cavia aperea and Galea musteloides , two closely related South-American rodents. In Cavia an extremely high incompatibility exists among adult males. As a consequence, only a single male can be kept together with several females even in richly structured enclosures of 20 m2. From this, a polygynous mating system emerges. In contrast, under similar housing conditions male Galea are much more tolerant and large groups can be established consisting of several adult males and several adult females. The mating system of Galea is promiscuous because of the female's soliciting behaviour when receptive that makes it impossible for a single male to monopolize her. The diverging mating systems correspond well with functional variations in testis size and sexual dimorphism: the polygynous Cavia show low testis masses (weight of both testes = 0.58% of body weight) and body weights are 11% higher in males than in nonpregnant females. The promiscuous Galea have extremely high relative testis masses (1.86% of body weight) and non-pregnant females are 15% heavier than males. In the latter species promiscuous mating results in a high percentage of multiple paternities (> 80% in groups of 4 males and 6-7 females) as revealed by multi-locus DNA fingerprinting. Nevertheless dominant males achieve a significantly higher reproductive success than subordinates. The high frequency of overt aggression directed from dominant to subordinate males, therefore, may be a mechanism to lower the fertilizing capacity of the lower ranking males. Concerning the females' reproductive success we demonstrated in a mating experiment that Galea which were paired with four males and became pregnant, weaned significantly more offspring than females which were paired with a single male. Thus, for the first time a reproductive benefit from promiscuous mating is shown for a female mammal. Field studies in the natural habitats of Cavia aperea and Galea musteloides are now performed to elucidate whether the differences in social and mating systems can be related to differences in ecological conditions.
Examined the effects of male removal on offspring survival and growth in the California mouse under 3 laboratory conditions: (1) warm ambient temperatures with food and water freely available, (2) warm ambient temperatures when parents were required to forage for food (i.e., wheel running), and (3) cold ambient temperatures with food and water freely available. The presence of the father had no effect on offspring survival in warm ambient temperatures, but father's presence enhanced infant survivorship in cold ambient temperatures and when parents had to forage to obtain food. Infants that survived, with or without their father, were similar in body mass from birth to weaning. Male care has probably evolved in this species because paternal investment enhances offspring survival under natural conditions. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
In biparental mating systems males are predicted to adjust their parental care in relation to their certainty of paternity. In this study, certainty of paternity in the European starling, Sturnus vulgaris, was manipulated by temporarily placing fertile females in cages next to decoy males within sight of their mates. Manipulations 2 weeks prior to egg laying provided a control, whilst watches on unmanipulated monogamous and polygynous pairs provided further comparison. Males did not respond to the manipulation by intensifying their mate guarding, but they did increase their song rates, which possibly reflected attempts to attract alternative females. No differences were observed between groups in any measures of mate guarding following the manipulation. There were significant sex differences in chick feeding rates within experimental pairs compared with controls owing to a reduction in male visits. Total visit rates and chick weights did not differ between experimental and control pairs. Visit rates in control pairs matched those of unmanipulated monogamous pairs, whereas those in experimental pairs did not differ from polygynous pairs. Low male visit rates were accompanied by a higher frequency of non-foraging activity around the colony, which was itself positively related to male song rates during the manipulations. It is suggested that this reflected a trade-off for males between chick feeding and time spent on additional mating opportunities, which would have been dependent on male 'quality' as indicated by song rate. Such a trade-off may have been crucial in producing the sex differences in chick feeding caused by the manipulation.
We measured potential advantages of living singly as contrasted to in male-female pairs in a free-living population of the prairie vole (Microtus ochrogaster) in a high food habitat. Whereas adult females survived longer when living in a pair than when living singly, adult males survived longer when single and wandering throughout the study site than when paired. Estimated total number of offspring produced that survived to adulthood and became reproductive was similar for paired females (0.32 female and 0.36 male offspring/female) and females living singly (0.34 female and 0.25 male offspring/female). There was no correlation between the proportion of unpaired adult males in the population and either adult population density, adult sex ratio, or proportion of females that were living singly. These results support the hypothesis that living in pairs evolved in the original low food habitat of the prairie vole and represents a basic behavioral trait that is retained regardless of food resources in the habitats now occupied.
1. The aim of this paper has been to review the theory behind kin recognition to examine the benefits individuals obtain by recognizing their kin and to review the mechanisms used by individuals in their recognition of kin.
2. The ability to discriminate between kin and non-kin, and between different classes of kin gives individuals advantages in fitness greater than individuals unable to recognize their kin. Four specific areas of benefit were considered: altruistic behaviour, co-operative behaviour, parental care and mate choice. Finally the possibility that kin recognition has arisen as a byproduct from some other ability was discussed.
3. Mechanisms of kin recognition were considered with respect to three essential components of kin recognition. The cue used to discriminate kin, how individuals classify conspecifics as kin, etc. and how the ability to recognize kin develops.
4. Individuals can use a number of cues to discriminate kin from non-kin. These were divided into cues presented by conspecifics (conspecific cues), of which three types were considered: individual, genetic and group/colony cues, and non-conspecific cues, environmental, state and no cues. Kin recognition could be achieved by use of all these cues.
5. How individuals classify their conspecifics as kin, etc. can be achieved in a number of ways; dishabituation or self-matching, which require no learning of kinship cues, or by phenotype matching or familiarity, both of which require the learning of kinship information.
6. It may be necessary for individuals to acquire information concerning kinship. This may be learned, and can be achieved in a number of ways; physiological imprinting, exposure learning or associative learning. Acquisition by these means is non-selective, in that the cues which are most salient in the individual's environment will be learned. Selectivity can be introduced into this process to increase the probability of acquiring kinship information by a number of means; learning from parents, sensitive periods for learning and prenatal learning. Finally, kinship information could be supplied by recognition genes.
7. A distinction is drawn between cues which are used by an individual in the discrimination of kin, discriminators, and cues which are used by individuals in the acquisition of information about kinship, acquisitors.
8. Experiments used to support previous categories of mechanisms of kin recognition were examined in the light of this discussion and it was found that the results were open to a number of different interpretations and yielded little specific information about the mechanisms of kin recognition.
9. It was concluded that there was much evidence, both theoretical and experimental to support the proposed benefits individuals gain from recognizing kin, but much more research is required before the mechanisms of kin recognition are fully understood.
Male investment in parental care has been hypothesized to be affected or not to be affected by their certainty of paternity, depending on the particular assumptions of theoretical models. We used data on paternal care and extra-pair paternity from 52 bird species to determine whether male parental care was related to certainity of paternity. Paternal care was measured as the relative male contribution to nest building, courtship feeding, incubation, and feeding of nestlings, respectively. Males of avian taxa did not provide less parental care during nest building, courtship feeding and incubation if the frequency of extra-pair paternity was high. However, male participation in feeding of offspring was significantly negatively related to the frequency of extra-pair paternity. This was also the case when the effects of potentially confounding variables such as developmental mode of offspring (which may result in males being freed from parental duties), extent of polygyny (which may result in less paternal care), and the frequency of multiple clutches during one breeding season (which may increase the probability of finding fertile females during the nestling period) were controlled statistically. These results suggest that the extent of paternal care has been affected by certainty of paternity, and that sex roles during the energetically most expensive parts of reproduction have been shaped by sperm competition.
Promiscuity is traditionally considered to increase only male reproductive success but, more recently, female benefits are also assumed to be the driving force for promiscuous mating. The yellow-toothed cavy (Galea musteloides) is characterised by an extremely high degree of multiple paternity (>80%), and females have greater offspring viability after mating multiple males. However, so far it is not clear whether or not it is the female's decision that leads to mating with more than one male. To elucidate the female's role in bringing about promiscuity, female yellow-toothed cavies were given the choice between four different males each, in a mate-choice apparatus that simultaneously prevented monopolisation and harassment of the females by the males. In 10 of the 12 choice tests, mating occurred. Nine of these ten females actively sought copulations with more than one male, and their mating behaviour was displayed in a way that might have favoured the mixing of sperm. At the same time, they significantly preferred heavier and more frequently courting males. These results show that female yellow-toothed cavies are actively involved in mating with more than one male. Thus, the present study is the first to show that in a species in which females produce more viable offspring as a consequence of polyandrous mating, these females are indeed motivated to actively bring about promiscuity. Nevertheless, females are selective in the choice of their mates. Thus, both sperm competition and direct female choice seem to be important for the increased offspring viability due to promiscuous mating.
In polyandrous dunnocks, natural variation in alpha versus beta male share of matings was correlated with their paternity share (assessed by DNA fingerpringting) and with their share of work in chick feeding. A polyandrous male's share of mating access was a better predictor of his parental effort than was his total amount of mating access, suggesting that a male might monitor his paternity share by comparing his mating success with that of his rival. Males were removed temporarily at various stages of the mating cycle to create experimental variation in mating success. The effects of this on paternity and male parental effort were compared, to test how well a male's chick-feeding behaviour promoted his own reproductive success. Fingerprinting revealed that replacement males sired most of the eggs fertilized during the removal period. Removed males fed chicks only if they had gained matings during egg laying. This behaviour was adaptive because of the greater loss of paternity to replacement males earlier on in the mating cycle, but it led males (1) to undervalue matings achieved before laying, which could fertilize the first eggs in the clutch, and (2) to overvalue later matings, achieved at a time when most or even all of the clutch was fertilized. The removals confirmed that the alpha: beta share of parental effort in polyandry was determined by their share of matings, not by their dominance rank per se. By contrast, experimental manipulation of a monogamous male's mating access did not influence his parental effort, despite paternity loss. Why responses differ in monogamy and polyandry, and why dunnocks do not pass on a paternity marker as a better guide to parental effort than these crude, indirect, cues based on mating access, are discussed.
The relationship between paternity and male parental behaviour was investigated in an eastern population of red-winged blackbirds. Data collected over four seasons revealed substantial variation in paternity and the frequency of male provisioning. The feeding of nestlings by males increased non-linearly with the age of the nestlings but did not differ within or between seasons. Average relative provisioning by males to individual nests was not associated with the proportion of nestlings sired by the territory owner (determined through multi-locus DNA fingerprinting), either in a bivariate analysis or a multivariate analysis with those variables found to be associated with male parental care in other studies of red-winged blackbirds. Males provisioned significantly less frequently at nests of older females, but paternity was not associated with female age. The later in the season a female settled, the higher her mate's paternity in her brood, yet male provisioning was not associated with female settlement date. Estimated total provisioning by males (sum of all feeding trips over all nests in each male's territory) was not associated with average paternity in bivariate and multivariate analyses. Total provisioning by males was positively associated with the number of days in the season the male had a brood in a bivariate test, but not with male age, the number of females nor male condition in either bivariate or multivariate analyses. The lack of a relationship between paternity and paternal effort fits predictions of recent theory on the potential effects of reduced paternity on paternal behaviour given (1) the lack of consistent patterns of paternity among nests of different order, time of season and male and female age and (2) generally weak associations between possible behavioural cues about paternity and actual paternity.
Paternal care in the monogamous swallow, Hirundo rustica, measured in terms of frequency of feeding of young, was positively related to the certainty of paternity. Male parental care increased with the absolute number of pair copulations and decreased with the absolute and relative number of extra-pair copulations by his mate. Nearly identical results were obtained using either relative or absolute number of male feedings as a measure of the intensity of parental care. Male swallows apparently estimated their certainty of paternity from the interest that neighbouring males were taking in their mates during the fertile period. When the number of extra-pair copulations involving their mates was experimentally increased, males significantly decreased their feeding rates compared with controls. Paternal care was not related to several measures of male quality (body condition, arrival time, mite infection, song rate, or mate guarding rate).
In Experiment I parental behavior was studied in 10 pairs of each of six species of muroid rodents: Microtus californicus, M. ochrogaster, M. californicus, M. montanus, Peromyscus maniculatus, and P. leucopus. Appreciable amounts of sitting on the nest, licking pups, and manipulating nesting materials were observed for all species, and manipulation and retrieval of pups for all Microtus species. Sex differences in parental behavior were relatively infrequent, reaching statistical significance in 9 of 60 comparisons. Species differences were significant in 58 of 150 comparisons for males and 46 of 150 for females. In Experiment II it was found that parity had little effect on parental behavior in the two Peromyscus species. These data both expand the catalog of species for which paternal behavior has been described and extend previous observations in several species. However, they provide little support for hypotheses that such behavior in the laboratory either is indicative of paternal behavior in the field or is a correlate of monogamous breeding systems, certainty of paternity, or adoption of a K-strategy in nature.
This review presents a systematic compilation of species in which only the male cares for the offspring. Such species occur rarely in the polychaetes, Hemiptera, Amphibia and birds and more often in the pycnogonids and fish. The facts are interpreted in the light of sexual selection theories. Care by only the male is more likely to occur if fertilization is external and might often be selected for as a consequence of site-attached behaviour by males. An explanation is suggested for the evolution of total role-reversal: it might result from the breakdown of a state of secondary equality of parental investment by the two sexes.
In many animals, males contribute substantially to caring for their young but also have the opportunity to enhance their reproductive success by attracting additional mates or by seeking copulations with females that are already paired to other males. Sometimes, the opportunity to gain these additional matings coincides with periods when males are providing parental care. At such times, males might be expected to allocate time and effort to these alternative behaviours in a way that maximizes their overall reproductive success. But do they? Here, we examine the recent evidence for a tradeoff between parental effort and additional mating effort and highlight some of the factors that might influence how this conflict is resolved. We conclude that, in spite of the paucity of comprehensive studies, this tradeoff has a potentially important and often overlooked influence on parental behaviour in a range of taxa.
It is generally believed that level of paternity (the proportion of zygotes in a brood that were fertilized by the male providing parental care) has an important role in the evolution of parental care. We have used population genetics models to investigate this role. The models indicate that only in mating systems where a parental male “sacrifices” promiscous matings can paternity influence the evolution of male parental care. This is because level of paternity can reflect the number of opportunities for these promiscuous fertilizations. For example, high paternity can mean few opportunities and therefore a low cost for paternal care.Certain behaviors may preadapt a species for the evolution of male parental care because they decrease the costs of providing care. For example, in fish species where male care has evolved from spawning territories, the very establishment of territories may have precluded males from gaining promiscuous matings, thereby eliminating the promiscuity costs and facilitating the evolution of care. Without a promiscuity cost, level of paternity will not have influenced the evolution of male care in fishes.Because paternity has limited influence in the evolution of male care, differences in reliability of parentage between males and females are unlikely to explain the prevalence of female care. Our analysis suggests that paternity differences between species cannot serve as a general explanation for the observed patterns of parental care behavior.
Male meadow voles, Microtus pennsylvanicus, were tested with unrelated pups to determine the social factors that affect the initiation of paternal responsiveness and the inhibition of infanticide. Adult males were initially more responsive to pups if they had been reared as neonates with their fathers rather than with unfamiliar males. Decreased aggression and facilitation of paternal responsiveness occurred most reliably after extensive exposure to pups, even if exposure had occurred more than 2 months before testing. Unlike house mice, neither copulation nor exposure to females enhanced male responsiveness to pups. Given that male meadow voles only nest with females and young during the colder parts of the breeding season, it may be adaptive for paternal responsiveness to be triggered by pup exposure, rather than by some aspect of earlier contact with the female.
When a male's paternity differs from one breeding attempt to another, the male's parental effort is expected to increase as paternity increases. Davies et al. (1992, Anim. Behav.43, 729–745) and Whittingham et al. (1993, Anim. Behav., 46, 139–147) manipulated paternity in monogamous dunnocks, Prunella modularis, and tree swallows, Tachycineta bicolor, respectively and found that parental effort did not vary with paternity. Previous discussions of this topic are reviewed and various examples presented to illustrate that the optimal parental effort may not depend strongly on paternity. In contrast to Whittingham et al., it is argued that the existing data do not indicate a discontinuous relationship between effort and paternity. Reasons to be sceptical about attempts to infer the shape of the relationship between parental effort and offspring survival from the form of the relationship between paternity and parental effort are also presented.
Conflicting data exist on the importance of the father and parental experience during development in rodents. The purpose of this study was to investigate the effects of these two variables on development in Mongolian gerbils. Forty pairs of males and females with a litter size of between 4 and 7 pups were used as subjects. Twenty couples had no experience in raising young. After the birth of their pups, four experimental groups were formed: (I) inexperienced mother and father; (II) inexperienced mother; (III) experienced mother and father and (IV) experienced mother. When the pups reached 10 days of age, pup and parental behavior was recorded in experimental sessions of 15 min on 11 consecutive days. Through the statistical analysis it was found that the presence of the father significantly increased the physical contact between pups and parents and that pups opened their eyes earlier in comparison to the groups without the father. On the other hand, parental experience had a significant influence on the behavior of the pups (locomotion inside and outside the nest, and self-grooming). The results of this study suggest that parental experience and the presence of the father have differentiated effects on development in Mongolian gerbils.
Parental effort by socially monogamous purple martins was measured to test the hypothesis that males reduce care in response to their risk of losing paternity through extra-pair copulations. Male martins occur in two age classes, with one-year-old males cuckolded in very high frequencies and older males achieving nearly complete paternity. This outcome is because females paired to young males pursue a mixed mating strategy of seeking extra-pair copulations, and females paired to old males avoid extra-pair copulations. Using multi-locus DNA fingerprinting to determine paternity, nb evidence was found that males reduced effort according to actual paternity or presumed confidence of paternity. Young and old males provisioned nestlings at similar rates in relative and absolute terms. There was also no relationship within the young age class, with young males provisioning similarly regardless of whether they were cuckolded. Young males achieving zero paternity provisioned similarly to young males achieving partial and complete paternity, suggesting that no threshold effect exists. Although several conditions have been proposed under which no relationship between paternity and male care is expected, these conditions did not exist for purple martins. Another condition under which males should not reduce care to unrelated offspring is proposed, namely, that performing poorly in the presence of potential future mates or extra-pair copulation partners can lower social status and thereby fitness. The 'status hypothesis' provides a perspective for viewing parental performance as a behavioural character on which sexual selection operates. (C) 1996 The Association for the Study of Animal Behaviour.