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Matriphagy in the hump earwig, Anechura harmandi (Dermaptera: Forficulidae), increases the survival rates of the offspring
Abstract
Females of the hump earwig, Anechura harmandi, are completely consumed by their offspring at the end of their care (matriphagy). The effect of this matriphagy was assessed by manipulative experiments. Matriphagy led to a delay in the dispersal of the nymphs and an increase in their survival rate. The same results were obtained when mothers were removed and the nymphs were given sufficient food. Females separated from their offspring after larval hatching failed to produce a second clutch, and three-quarters of them did not develop their ovaries. These results suggest that the survival of nymphs and their stay in the nest are dependent on food availability and that A. harmandi females are strictly semelparous.
... The females survive for a month after spawning, during which time they brood their eggs (which are otherwise unprotected) and generally die a few days after the eggs hatch (Wodinsky 1977;Van Heukelem 1983). Semelparous female salmon arriving early at their spawning grounds have a longer post-spawning survival (to guard their nests so that the site cannot be reused, which would drastically reduce the survival of her eggs) than late-arriving females Matriphagy has been reported in some species of insects (Kohno 1997;Pollock & Normark 2002;Suzuki et al. 2005) and spiders (Evans et al. 1995;Kim et al. 2000;Toyama 1999Toyama , 2001). Matriphagy is not only an extreme form of semelparous maternal care but also a paradigmatic joint process of fitness transfers by both parental care and parental demise. ...
... In several arthropod species, semelparous females care for their young and are finally consumed entirely by their offspring (Schneider 1996;Kim et al. 2000;Toyama 2001;Suzuki et al. 2005). Parental provisioning significantly improves offspring survival and development (Yip & Rayor 2014). ...
... Amaurobius ferox spiderlings had higher survival and moulted earlier when they could feed on the mother (Kim et al. 2000). Likewise, matriphagy increases offspring survival in the hump earwig Anechura harmandi (Suzuki et al. 2005). Females of the Japanese foliage spider, Chiracanthium japonicum, are eaten by their offspring at the end of the maternal care period (Toyama 2003). ...
... In addition, Smith and Charnov (2001) presented evidence that in a small rodent, Neotoma lepida, adaptations to an increasingly harsh environment during the early Holocene favored a switch from iteroparity to semelparity. Likewise, in the strictly semelparous hump earwig Anechura harmandi (Suzuki et al. 2005) unfavorable environmental conditions seemed to have a large effect on the evolution of semelparity and cannibalism in this species (Kohno 1997). Matriphagy appears to play an important role in ensuring early adult emergence and survival in nymphs of A. harmandi because they can start development early in the spring when the food resource may still be scarce (Kohno 1997;Suzuki et al. 2005). ...
... Likewise, in the strictly semelparous hump earwig Anechura harmandi (Suzuki et al. 2005) unfavorable environmental conditions seemed to have a large effect on the evolution of semelparity and cannibalism in this species (Kohno 1997). Matriphagy appears to play an important role in ensuring early adult emergence and survival in nymphs of A. harmandi because they can start development early in the spring when the food resource may still be scarce (Kohno 1997;Suzuki et al. 2005). ...
... istic of this order is that all earwig species in it studied to date exhibit maternal care, especially those in the suborder Forficulina (Lamb 1976;Costa 2006). Although this order is not very large, the extent of care varies greatly among its species (Vancassel 1984), ranging from egg guarding only (Matzke & Klass 2005;Shimizu & Machida 2011) to provisioning of nymphs (Staerkle & Kölliker 2008;Suzuki 2010), matriphagy (Kohno 1997;Suzuki et al. 2005), and ovoviviparity (Kamimura et al. 2016). This variation can be found among species within the same family, or even among those in the same genus (e.g., in the genus Anechura; Vancassel & Forasé 1980;Kohno 1997;Suzuki et al. 2005 see also Costa 2006). ...
... Although this order is not very large, the extent of care varies greatly among its species (Vancassel 1984), ranging from egg guarding only (Matzke & Klass 2005;Shimizu & Machida 2011) to provisioning of nymphs (Staerkle & Kölliker 2008;Suzuki 2010), matriphagy (Kohno 1997;Suzuki et al. 2005), and ovoviviparity (Kamimura et al. 2016). This variation can be found among species within the same family, or even among those in the same genus (e.g., in the genus Anechura; Vancassel & Forasé 1980;Kohno 1997;Suzuki et al. 2005 see also Costa 2006). ...
... Nevertheless, many important studies published in recent years require updates. They include studies on the costs and benefits of maternal care (Suzuki et al. 2005;Kölliker 2007;Kölliker & Vancassel 2007;Miller et al. 2011;Meunier & Kölliker 2012a;Miller & Zink 2012), cannibalism among family members (Suzuki et al. 2005;Dobler & Kölliker 2010;Miller & Zink 2012), provisioning behavior and its regulation (Staerkle & Kölliker 2008;Mas et al. 2009;Suzuki 2010Suzuki , 2011Mas & Kölliker 2011;Meunier & Kölliker 2012b;Wong & Kölliker 2012), evolution of the number of reproductive cycles (Meunier et al. 2012), possible viviparity in a tropical species (Kočárek 2009) and reproduction in poorly known primitive representative species (Matzke & Klass 2005;Shimizu & Machida 2009. Second, earwigs are characterized by their forceps, which are specialized cerci located at the caudal end of the abdomen (Fig. 1A-E). ...
... Nevertheless, many important studies published in recent years require updates. They include studies on the costs and benefits of maternal care (Suzuki et al. 2005;Kölliker 2007;Kölliker & Vancassel 2007;Miller et al. 2011;Meunier & Kölliker 2012a;Miller & Zink 2012), cannibalism among family members (Suzuki et al. 2005;Dobler & Kölliker 2010;Miller & Zink 2012), provisioning behavior and its regulation (Staerkle & Kölliker 2008;Mas et al. 2009;Suzuki 2010Suzuki , 2011Mas & Kölliker 2011;Meunier & Kölliker 2012b;Wong & Kölliker 2012), evolution of the number of reproductive cycles (Meunier et al. 2012), possible viviparity in a tropical species (Kočárek 2009) and reproduction in poorly known primitive representative species (Matzke & Klass 2005;Shimizu & Machida 2009. Second, earwigs are characterized by their forceps, which are specialized cerci located at the caudal end of the abdomen (Fig. 1A-E). ...
Dermaptera (earwigs) is a relatively small polyneopteran order with approximately 2200 described species. They are characterized by a pair of forceps, which are hardened, unsegmented cerci at the caudal end of the abdomen. In most species, males have more exaggerated forceps than females, indicating an effect of sexual selection on them. Earwigs also exhibit astonishing diversity in the number, laterality and size of both male and female genital components. This characteristic has promoted the study of postcopulatory sexual selection in several representative species. Here, previous studies of earwigs that examined pre- and postcopulatory sexual selection are reviewed in detail. Related topics included here are sexually antagonistic coevolution, evolution of laterally asymmetrical morphologies, and developmental aspects of intra-sexually dimorphic traits. A new terminology system for male genitalia is also proposed.
... An extreme form of care that may occur under very low food availability is matriphagy. In the hump earwig (Anechura harmandi ), an obligatory matriphagous species, first-instar nymphs kill and eat their mother before dispersing from the nest (Kohno, 1997;Suzuki et al ., 2005). Hump earwig mothers do not seem to attempt escape from cannibalism by their nymphs and even do not produce a second clutch when being experimentally isolated from their nymphs. ...
... Hump earwig mothers do not seem to attempt escape from cannibalism by their nymphs and even do not produce a second clutch when being experimentally isolated from their nymphs. Thus, matriphagy provides important benefits to the offspring while the costs for the female seem very low due to the low chances of future reproduction (Suzuki et al ., 2005). Also, anatomical/morphological adaptations by parents may enhance offspring fitness under harsh physical conditions. ...
1. Parental care increases the fitness of offspring at a cost to the parents in terms of residual reproductive success. This trade-off may be affected by ecology, life history and the social environment, which raises the question as to how these factors contribute to the evolution of parental care. Here, previous hypotheses concerning the evolution of parental care in insects are summarized and discussed and the underlying empirical evidence is reviewed. 2. Ecological factors such as harsh environments, ephemeral food sources or predation pressure are broadly accepted as evolutionary drivers of parental care. The most consistent evidence supports a role for natural enemies such as predators, microbes and cannibalistic conspecifics. Also, the importance of ecological factors may interact with the life history (parity) of a species, either as a pre-adaptation facilitating the evolution of parental care or as a consequence of enhanced parental investment under parental care. Yet, only limited experimental research has been carried out to test the combined influence of ecology and life history in the evolution of parental care. 3. Several forms of care can mediate the transition from solitary to family living, which entails the emergence of a novel – social – environment that generates new selection pressures from interactions within and between families. In this context, we review examples of studies on communal breeding, brood parasitism, parent–offspring conflict and co-adaptation, and discuss how these social interactions may in turn be influenced by ecological factors such as food availability or population density. 4. Insects are uniquely suitable for experimental and comparative research on the complex interplay between ecology, life history, and the social environment.
... Tended larvae left their nest much less, a result that confirms a recent field study in the same species (Kölliker and Vancassel 2007). This result is in line with the hypothesis that it may be adaptive for unattended sub-social insect larvae to leave the nest early, disperse to forage independently or join (and ideally get adopted by) other intact family groups (Agrawal et al. 2004; Suzuki et al. 2005; Kölliker and Vancassel 2007). A recent study in the hump earwig Anechura harmandi showed that the early larval dispersal triggered by maternal absence was due to the resulting food shortage. ...
... A recent study in the hump earwig Anechura harmandi showed that the early larval dispersal triggered by maternal absence was due to the resulting food shortage. When food was experimentally added, larval dispersal could be restored to the usual level even in the absence of the mother (Suzuki et al. 2005). In the present study, independent foraging by larvae seemed to be quite efficient (note that, to attain the food source, larvae had to leave the burrow). ...
The evolution of parental care and family group formation critically depends on offspring survival benefits and parental fecundity
costs of care under given ecological conditions. Investigations of the functional significance of care in insect species that
exhibit facultative parental care have been relatively rare but may be of particular interest for better understanding of
benefit and cost schedules at an early evolutionary stage. In this study, aspects of benefits and costs of care were addressed
in the sub-social European earwig (Forficula auricularia; Dermaptera: Forficulidae) by manipulating the presence of tending mothers and brood size in a fully crossed experimental
design. Larvae growing in broods tended by their mother or of reduced size showed a higher survival probability than larvae
growing in untended or large broods, as predicted if maternal care is beneficial and shaped by a trade-off between number
and quality of offspring. Analysis of patterns of food consumption and developmental time further suggested that the benefit
of maternal attendance is mediated by the maternal provisioning of food, while the quality–quantity trade-off seemed to be
driven by sibling rivalry. Further, tending mothers delayed the production of a second clutch, indicating a potential cost
of care in terms of lifetime fecundity. This study experimentally shows benefits and potential costs of maternal care and
family group formation in the European earwig. More detailed behavioural experiments will be required to fully understand
how behavioural interactions among family members mediate these reproductive outcomes.
... Finally, an extreme form of parental food provisioning occurs when parents provision their offspring with their bodies. This rare phenomenon has been reported in the hump earwig, Anechura harmandi, where offspring completely consume their mother at the end of post-hatching care (Suzuki et al., 2005). Matriphagy also occurs in the beetle Micromalthus debilis, the sole species of the family Micromalthidae. ...
... The majority of earwigs are oviparous, whereas the epizoic groups are viviparous, i.e., directly giving birth to nymphs. Besides, unusual maternal care behavior is found in all studied earwig species, with the female protecting eggs and first-instar nymphs (Suzuki et al. 2005;Staerkle and Koelliker 2008). ...
The phylogenetic position and inner relationships of Dermaptera remain unresolved despite the numerous efforts using morphological and molecular data. To facilitate the resolution of problems, this study sequenced the complete mitogenome of Apachyus feae de Bormans, 1894 (Apachyidae) and the nearly complete mitogenome of Diplatys flavicollis Shiraki, 1907 (Diplatyidae). The 19,029-bp long mitogenome of A. feae exhibited an extra trnV gene and two control regions in addition to the typical set of 37 genes including 13 protein-coding genes (PCGs), 22 transfer RNA (tRNA) genes, and two ribosomal RNA (rRNA) genes. The 12,950-bp long partially sequenced mitogenome of D. flavicollis was composed of 10 and a partial fragment of PCGs, 18 tRNA genes, two rRNA genes, and a control region. Comparative analysis of available earwig mitogenomes revealed variable mitogenomic structure and extensive gene rearrangements in Dermaptera. The preliminary phylogenetic analyses using Bayesian inference and maximum likelihood methods showed identical results, but the limited sampling and different types of molecular data lead to an apparent incongruence with previous phylogenetic studies.
... Finally, an extreme form of parental food provisioning occurs when parents provision their offspring with their bodies. This rare phenomenon has been reported in the hump earwig, Anechura harmandi, where offspring completely consume their mother at the end of post-hatching care (Suzuki et al., 2005). Matriphagy also occurs in the beetle Micromalthus debilis, the sole species of the family Micromalthidae. ...
Among the multiple strategies that males and females can adopt to ensure the proper development of their offspring, an important one is the expression of parental care. Following Smiseth et al. (2012), parent care is defined as ‘any parental trait that enhances the fitness of a parent’s offspring, and that is likely to have originated and/or is currently maintained for this function’. This broad definition of parental care encompasses behavioural (e.g. egg grooming) as well as non-behavioural (e.g. provi-sioning of gametes) traits that may be expressed both before and after oviposition, but excludes traits whose bearers are individuals other than the parents (e.g. adult siblings). In nature, parental care can take a broad diversity of forms, ranging from egg provisioning and nest construction over brood at-tendance to food provisioning (Clutton-Brock, 1991; Costa, 2006; Smiseth et al., 2012; Wong et al.,2013). The diverse forms of care can be provided by either the mother, the father or both parents; they can last from only few minutes to several years; and can range from mildly beneficial to essential for offspring survival (Klug et al., 2012; Trumbo, 2012; Kramer & Meunier, 2019). Regardless of its form, parental care often has a profound impacts on the fitness of both offspring and parents. On the one hand, parental care is beneficial to offspring, as it can improve their quality and increase their survival by neutralizing environmental hazards (Alonso‐Alvarez & Velando, 2012; Klug & Bonsall, 2014). On the other hand, investing into parental care often comes with costs to parents. This is because its expression negatively impacts the condition and survival of the tending parents (due to an
increased energy loss or elevated risk of predation), and thus reduces their lifetime reproductive success (Trivers, 1972; Alonso-Alvarez & Velando, 2012).......
... Parental care requires investment in time and energy by one or both parents (Wong et al. 2013) and involves costs that can affect future reproductive events (Zink 2003a) and the survivorship of parents (Suzuki et al. 2005). These costs may be compensated if offspring survival increases as a consequence of parental care, thereby increasing the indirect fitness of one or both parents (Wong et al. 2013;Hamilton 1964;Alonzo and Klug 2012). ...
Alchisme grossa is a treehopper species showing maternal care until at least the third nymphal instar. A secondary female treehopper has frequently been observed near a family (primary female guarding its egg clutch). Intraspecific brood parasitism, communal breeding or alloparental care may be suggested as possible mechanisms to explain secondary female presence. To distinguish between these phenomena, we performed relatedness analyses of genetic samples of groups including one A. grossa primary female, a secondary female and the associated offspring using polymorphic microsatellites. Furthermore, we characterized the behavioral interaction between both females during maternal care and the reproductive strategy (monandry or polyandry) of A. grossa females by estimating the number of male parents. We observed the presence of secondary females in 35.9% of monitored families. The behaviors characterized suggest the occurrence of brood parasitism in the interaction between both females. Nevertheless, all offspring within a family were descendants only of the primary female and a single male, thus showing that A. grossa females are monandrous. The results, taken together with data on the reproductive biology reported for other treehoppers, are consistent with the occurrence of brood parasitism in A. grossa.
... The mother protects the eggs from predators as well as clean them to reduce fungal growth. They also feed the first instar larvae with regurgitated food (Staerkel and Koelliker, 2008;Suzuki et al., 2005;Naegel et al., 2016). ...
Order Dermaptera, commonly known as "earwigs" comprise about 1,942 species globally. A total of 152 species belonging to 52 genera and seven families are reported from the Indian Himalaya, of which 28.9% of the species are endemic to the region. Among different biotic provinces within Indian Himalaya biogeographic zone, East Himalaya has the highest species richness (84) followed by Central Himalaya (77) and West Himalaya (56).
... This discussion may be usefully extended to other examples of matriphagy, as occurs for example in a number of species of insects and spiders, where it has been shown to increase fitness not only of offspring but also of mothers (Salomon et al., 2005;Suzuki et al., 2005). This is illustrated by the black lace-weaver spider (Amaurobius ferox) where mothers that are cannibalized have higher fitness than those that are not and go on to produce a second clutch (Kim et al., 2001). ...
A widely appreciated conclusion from evolutionary theory is that senescence (aging) is of no adaptive value to the individual that it afflicts. Yet studies of Caenorhabditis elegans and Saccharomyces cerevisiae are increasingly revealing the presence of processes which actively cause senescence and death, leading some biogerontologists to wonder about the established theory. Here we argue that programmed death that increases fitness could occur in C. elegans and S. cerevisiae, and that this is consistent with the classic evolutionary theory of aging. This is because of the special conditions under which these organisms have evolved, particularly the existence of clonal populations with limited dispersal and, in the case of C. elegans, the brevity of the reproductive period caused by protandrous hermaphroditism. Under these conditions, death-promoting mechanisms could promote worm fitness by enhancing inclusive fitness, or worm colony fitness through group selection. Such altruistic, adaptive death is not expected to evolve in organisms with outbred, dispersed populations (e.g. most vertebrate species). The plausibility of adaptive death in C. elegans is supported by computer modelling studies, and new knowledge about the ecology of this species. To support these arguments we also review the biology of adaptive death, and distinguish three forms: consumer sacrifice, biomass sacrifice and defensive sacrifice.
... Actual copulation in earwigs can take several hours and can be repeated before the male and female separate. Suzuki et al. (2005) examined maternal care in Anechura harmandi and found that matriphagy increases the survival rates of nymphs. However, matriphagy and semelparity are the exception in Dermaptera, as many females can have more than one brood if climatic conditions allow. ...
The Dermaptera, or earwigs, are a small group of medium‐sized insects (typically 10‐15 mm long), with more than 1900 described, living species, although only a few are known to the general public. The most significant departures from typical earwigs are the Arixeniidae and Hemimeridae, two distinct and unrelated epizoic Dermaptera groups. Both families convergently evolved a close relationship with mammals. Development in Dermaptera is hemimetabolous, with an egg stage, 4‐6 nymphal instars, and the adult stage. Maternal care and mating have attracted most of the research on dermapteran behavior. At present, there is considerable interest in the Dermaptera, covering almost all aspects, including structure, function, and behavior. Dermaptera show aggregation behavior, whereby conspecific animals gather together. This behavior is mediated by an aggregation pheromone. Dermapteran phylogeny is somewhat unstable, and the distinction between lower and higher Dermaptera is arbitrary, although based on similarities in lifestyle and distribution.
... When the temporal window for breeding is limited, or juvenile survival is highly predictable and adult survival low (Stearns 1992;Lessells 2005), extreme investment in current reproduction may be selected at the expense of all future reproduction. As a result, semelparity can occur in one (e.g., Bradley et al. 1980;Huse 1998;Fromhage et al. 2005;Suzuki et al. 2005;Bonnet 2011;Fisher and Blomberg 2011) or both sexes (Hendry et al. 1999). In systems with sex-specific semelparity, the semelparous sex is expected to invest minimally in survival beyond maturity (e.g., Bonnet 2011;Fisher et al. 2013) and thus to exhibit a Bfaster^pace of life. ...
Males and females commonly differ in their life history optima and, consequently, in the optimal expression of life history, behavioral and physiological traits involved in pace-of-life syndromes (POLS). Sex differences in mean trait expression typically result if males and females exhibit different fitness optima along the same pace-of-life continuum, but the syndrome structure may also differ for the sexes. Due to sex-specific selective pressures imposed by reproductive roles and breeding strategies, the sexes may come to differ in the strength of correlation among traits, or different traits may covary in males and females. Ignorance of these selective forces operating between and within the sexes may lead to flawed conclusions about POLS manifestation in the species, and stand in the way of understanding the evolution, maintenance, and variability of POLS. We outline ways in which natural and sexual selection influence sex-specific trait evolution, and describe potential ultimate mechanisms underlying sex-specific POLS. We make predictions on how reproductive roles and the underlying sexual conflict lead to sex-specific trait covariances. These predictions lead us to conclude that sexual dimorphism in POLS is expected to be highly prevalent, allow us to assess possible consequences for POLS evolution, and provide guidelines for future studies.
... Maternal care such as egg guarding and larval tending is, in some insect species, followed by matriphagy, which serves to increase larval survival. Matriphagy has been observed in the bizarrely complex life cycle of the telephone beetle, Micromalthus debilis LeConte (Pollack and Normark 2002), and also in certain earwigs (Suzuki et al. 2005) and Stegodyphus lineatus (Laetreille) spiders (Salomon et al. 2015). The deaths (after five to 11 days) of all first instar larvae appeared to be caused by the refusal of the larvae to eat any of the offered foods. ...
Over 13 seasons, from 1992 to 2016, field studies detailing the life habits of Phausis inaccensa LeConte were carried out primarily in Mississippi and Tennessee with additional data from Arkansas, Pennsylvania, North Carolina, and Minnesota. From late March to May in the southern states, ≈45 minutes after sunset, apterous, neotenic females emerge from their daytime shelters in the leaf litter, glow from two spots at the end of their upturned abdomens, and attract flying, lanternless males. Signaling females, often in loose groupings of three to four, attract multiple males that land near (60 mm, SD 15) but not directly on them. Male activity was greatest from 30 to 60 minutes after sunset, and ended by two hours past sunset. Unmated females displayed longer (from 90 minutes to all night) than the mated females, which typically displayed for a shorter time. Eighty percent of the females signaled and mated on a single night. Mating durations were brief, averaging eight minutes when one male was present, but significantly longer (12-45 minutes) when more than one male was present. In captivity, both males and females mated multiple times. More than 90% of the males and 70% of the females were active during the three-week period that equaled about 450-500 modified growing degree days Fahrenheit. Northern populations showed a different seasonality, but similar habits. Females lived an average of 14 days in captivity, oviposited clutches of 20-30 round pale eggs, 0.5 mm diameter, and exhibited maternal care and guarding of their eggs until their death six to nine days after oviposition. Larvae, 1.57 mm, emerged in 34-37 days. We compare these observations with similar and often sympatric Phausis reticulata Say, the Blue Ghost firefly, whose males glow during their flights in search of females. © The Author 2017. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved.
... In spiders, matriphagy has evolved independently in Amaurobiidae, Eresidae, Theridiidae, and Thomisidae (Pekar 2000;Yip & Rayor 2013). Similar processes may occur in other taxa exhibiting suicidal maternal care such as the hump earwig Anechura harmandi Burr 1904 (Suzuki et al. 2005). ...
Parental care entails physiological costs to the mother. These costs, even if dramatic, are usually reversible and do not result in mortality of the mother. In the spider Stegodyphus lineatus Latreille 1817 (Eresidae), maternal care is extreme and irreversible: mothers regurgitate food for the young and then die when consumed by them (matriphagy). We examined whether the mother's midgut tissues undergo structural changes in preparation for regurgitation and matriphagy. Our histological data show that the midgut diverticula (MD) tissues start to degrade during the egg sac incubation period. When the young emerge from the egg sac, the midgut tissues are partly liquefied and are retained within the MD. The degradation process intensifies when the female feeds her young by regurgitation and liquid tissue is observed within and among the diverticula lobes. The presence of the lumen of a diverticulum during the regurgitation process suggests that degenerated tissues enter the lumen and form the regurgitated fluid. At matriphagy, the abdomen is filled with liquid containing nutritional vacuoles, which the young imbibe after piercing the female's abdomen. We conclude that the MD undergoes a gradual degradation process that maximizes the nutritional potential of the female's body and finally enables complete consumption of her soma. These changes are consistent with the extreme semelparous reproductive system of S. lineatus, where a female invests all of her resources into a single reproductive event. This is the first demonstration of the mechanism underlying suicidal maternal care in an arthropod. Raising offspring is costly, and investment in parental care may be traded off against future reproduction (Fox & Csezak 2000). A major cost of parental care is the physiological burden on the mother. Maternal care in spiders may be transient or extended (Yip & Rayor 2013). Transient maternal care is widespread in spiders and is mainly restricted to protection of egg sacs or of the young until dispersal shortly after emergence (Lubin & Bilde 2007). Extended maternal care of offspring after emergence from the egg sac (subsocial behavior) has evolved multiple times, and occurs in at least 65 species in 16 families (Yip & Rayor 2013). The behaviors include feeding the young with captured prey (Gundermann et al. 1988; Schneider 1996), producing trophic oocytes (Gun-dermann et al. 1991; Evans et al. 1995), regurgitating food for the young (Kullmann & Zimmerman 1975) and matriphagy, i.e. the consumption of the mother by her young (Seibt & Wickler 1987; Kim & Horel 1998; Kim et al. 2000). While transient maternal care does not restrict the production of additional broods, extended maternal care, such as providing prey for the young, regurgitation feeding, and production of trophic eggs involve prolonged association between the mother and her brood and may constrain the female to a single clutch (Yip & Rayor 2014). Matriphagy is an extreme form of maternal investment and is an irreversible dead-end for the mother that precludes the possibility of future reproduction. Do such constraints on future reproduction involve changes in physiology and internal anatomy that at some stage become irreversible? Female Stegodyphus lineatus Latreille 1817 (Eresidae) exhibits intensive maternal care for newly emerged young, first by regurgitating liquid food and later by allowing matriphagy. Females lay a single clutch of ,80 eggs that constitutes less than 3% of the body mass of the mother at oviposition (Schneider 1996), and will lay a second clutch of eggs only if the first is lost due to predation or male infanticide (Schneider & Lubin 1997a). After emergence of the young, the female provides the young with regurgitated fluid (Kullmann & Zimmermann 1975). Young of females fed with radioactive flies became radioactive a few days after emergence, indicating a transfer of digested prey from the mother to her young (Kullmann 1972). After two weeks of regurgitation feeding, the young climb on the mother's body and consume her (matriphagy; Seibt & Wickler 1987); within 2–3 hours they extract her body fluids leaving behind only a dry exoskeleton (Salomon et al. 2005). In this species, the mother ceases to eat after the young emerge. She does not provide prey to the young and the young are incapable of catching and ingesting prey independently, and thus they will die without her regurgitated fluid (Salomon & Lubin unpubl. data). Therefore , the body mass of the female at the emergence of the young constitutes all the food available for the young during maternal care. During regurgitation, the female loses 41% of her body mass, while in matriphagy, the young consume an additional 54% of her body mass measured at emergence of the young. Thus a total of 95% of her body mass is provided to the young as food (Salomon et al. 2005). These maternal care behaviors lead to a threefold increase in the body mass of
... In spiders, matriphagy has evolved independently in Amaurobiidae, Eresidae, Theridiidae, and Thomisidae (Pekar 2000;Yip & Rayor 2013). Similar processes may occur in other taxa exhibiting suicidal maternal care such as the hump earwig Anechura harmandi Burr 1904 (Suzuki et al. 2005). ...
Parental care entails physiological costs to the mother. These costs, even if dramatic, are usually reversible and do not result in mortality of the mother. In the spider Stegodyphus lineatus Latreille 1817 (Eresidae), maternal care is extreme and irreversible: mothers regurgitate food for the young and then die when consumed by them (matriphagy). We examined whether the mother's midgut tissues undergo structural changes in preparation for regurgitation and matriphagy. Our histological data show that the midgut diverticula (MD) tissues start to degrade during the egg sac incubation period. When the young emerge from the egg sac, the midgut tissues are partly liquefied and are retained within the MD. The degradation process intensifies when the female feeds her young by regurgitation and liquid tissue is observed within and among the diverticula lobes. The presence of the lumen of a diverticulum during the regurgitation process suggests that degenerated tissues enter the lumen and form the regurgitated fluid. At matriphagy, the abdomen is filled with liquid containing nutritional vacuoles, which the young imbibe after piercing the female's abdomen. We conclude that the MD undergoes a gradual degradation process that maximizes the nutritional potential of the female's body and finally enables complete consumption of her soma. These changes are consistent with the extreme semelparous reproductive system of S. lineatus, where a female invests all of her resources into a single reproductive event. This is the first demonstration of the mechanism underlying suicidal maternal care in an arthropod. Raising offspring is costly, and investment in parental care may be traded off against future reproduction (Fox & Csezak 2000). A major cost of parental care is the physiological burden on the mother. Maternal care in spiders may be transient or extended (Yip & Rayor 2013). Transient maternal care is widespread in spiders and is mainly restricted to protection of egg sacs or of the young until dispersal shortly after emergence (Lubin & Bilde 2007). Extended maternal care of offspring after emergence from the egg sac (subsocial behavior) has evolved multiple times, and occurs in at least 65 species in 16 families (Yip & Rayor 2013). The behaviors include feeding the young with captured prey (Gundermann et al. 1988; Schneider 1996), producing trophic oocytes (Gun-dermann et al. 1991; Evans et al. 1995), regurgitating food for the young (Kullmann & Zimmerman 1975) and matriphagy, i.e. the consumption of the mother by her young (Seibt & Wickler 1987; Kim & Horel 1998; Kim et al. 2000). While transient maternal care does not restrict the production of additional broods, extended maternal care, such as providing prey for the young, regurgitation feeding, and production of trophic eggs involve prolonged association between the mother and her brood and may constrain the female to a single clutch (Yip & Rayor 2014). Matriphagy is an extreme form of maternal investment and is an irreversible dead-end for the mother that precludes the possibility of future reproduction. Do such constraints on future reproduction involve changes in physiology and internal anatomy that at some stage become irreversible? Female Stegodyphus lineatus Latreille 1817 (Eresidae) exhibits intensive maternal care for newly emerged young, first by regurgitating liquid food and later by allowing matriphagy. Females lay a single clutch of ,80 eggs that constitutes less than 3% of the body mass of the mother at oviposition (Schneider 1996), and will lay a second clutch of eggs only if the first is lost due to predation or male infanticide (Schneider & Lubin 1997a). After emergence of the young, the female provides the young with regurgitated fluid (Kullmann & Zimmermann 1975). Young of females fed with radioactive flies became radioactive a few days after emergence, indicating a transfer of digested prey from the mother to her young (Kullmann 1972). After two weeks of regurgitation feeding, the young climb on the mother's body and consume her (matriphagy; Seibt & Wickler 1987); within 2–3 hours they extract her body fluids leaving behind only a dry exoskeleton (Salomon et al. 2005). In this species, the mother ceases to eat after the young emerge. She does not provide prey to the young and the young are incapable of catching and ingesting prey independently, and thus they will die without her regurgitated fluid (Salomon & Lubin unpubl. data). Therefore , the body mass of the female at the emergence of the young constitutes all the food available for the young during maternal care. During regurgitation, the female loses 41% of her body mass, while in matriphagy, the young consume an additional 54% of her body mass measured at emergence of the young. Thus a total of 95% of her body mass is provided to the young as food (Salomon et al. 2005). These maternal care behaviors lead to a threefold increase in the body mass of
... In spiders, matriphagy has evolved independently in Amaurobiidae, Eresidae, Theridiidae, and Thomisidae (Pekar 2000;Yip & Rayor 2013). Similar processes may occur in other taxa exhibiting suicidal maternal care such as the hump earwig Anechura harmandi Burr 1904 (Suzuki et al. 2005). ...
Parental care entails physiological costs to the mother. These costs, even if dramatic, are usually reversible and do not result in mortality of the mother. In the spider Stegodyphus lineatus Latreille 1817 (Eresidae), maternal care is extreme and irreversible: mothers regurgitate food for the young and then die when consumed by them (matriphagy). We examined whether the mother's midgut tissues undergo structural changes in preparation for regurgitation and matriphagy. Our histological data show that the midgut diverticula (MD) tissues start to degrade during the egg sac incubation period. When the young emerge from the egg sac, the midgut tissues are partly liquefied and are retained within the MD. The degradation process intensifies when the female feeds her young by regurgitation and liquid tissue is observed within and among the diverticula lobes. The presence of the lumen of a diverticulum during the regurgitation process suggests that degenerated tissues enter the lumen and form the regurgitated fluid. At matriphagy, the abdomen is filled with liquid containing nutritional vacuoles, which the young imbibe after piercing the female's abdomen. We conclude that the MD undergoes a gradual degradation process that maximizes the nutritional potential of the female's body and finally enables complete consumption of her soma. These changes are consistent with the extreme semelparous reproductive system of S. lineatus, where a female invests all of her resources into a single reproductive event. This is the first demonstration of the mechanism underlying suicidal maternal care in an arthropod. Raising offspring is costly, and investment in parental care may be traded off against future reproduction (Fox & Csezak 2000). A major cost of parental care is the physiological burden on the mother. Maternal care in spiders may be transient or extended (Yip & Rayor 2013). Transient maternal care is widespread in spiders and is mainly restricted to protection of egg sacs or of the young until dispersal shortly after emergence (Lubin & Bilde 2007). Extended maternal care of offspring after emergence from the egg sac (subsocial behavior) has evolved multiple times, and occurs in at least 65 species in 16 families (Yip & Rayor 2013). The behaviors include feeding the young with captured prey (Gundermann et al. 1988; Schneider 1996), producing trophic oocytes (Gun-dermann et al. 1991; Evans et al. 1995), regurgitating food for the young (Kullmann & Zimmerman 1975) and matriphagy, i.e. the consumption of the mother by her young (Seibt & Wickler 1987; Kim & Horel 1998; Kim et al. 2000). While transient maternal care does not restrict the production of additional broods, extended maternal care, such as providing prey for the young, regurgitation feeding, and production of trophic eggs involve prolonged association between the mother and her brood and may constrain the female to a single clutch (Yip & Rayor 2014). Matriphagy is an extreme form of maternal investment and is an irreversible dead-end for the mother that precludes the possibility of future reproduction. Do such constraints on future reproduction involve changes in physiology and internal anatomy that at some stage become irreversible? Female Stegodyphus lineatus Latreille 1817 (Eresidae) exhibits intensive maternal care for newly emerged young, first by regurgitating liquid food and later by allowing matriphagy. Females lay a single clutch of ,80 eggs that constitutes less than 3% of the body mass of the mother at oviposition (Schneider 1996), and will lay a second clutch of eggs only if the first is lost due to predation or male infanticide (Schneider & Lubin 1997a). After emergence of the young, the female provides the young with regurgitated fluid (Kullmann & Zimmermann 1975). Young of females fed with radioactive flies became radioactive a few days after emergence, indicating a transfer of digested prey from the mother to her young (Kullmann 1972). After two weeks of regurgitation feeding, the young climb on the mother's body and consume her (matriphagy; Seibt & Wickler 1987); within 2–3 hours they extract her body fluids leaving behind only a dry exoskeleton (Salomon et al. 2005). In this species, the mother ceases to eat after the young emerge. She does not provide prey to the young and the young are incapable of catching and ingesting prey independently, and thus they will die without her regurgitated fluid (Salomon & Lubin unpubl. data). Therefore , the body mass of the female at the emergence of the young constitutes all the food available for the young during maternal care. During regurgitation, the female loses 41% of her body mass, while in matriphagy, the young consume an additional 54% of her body mass measured at emergence of the young. Thus a total of 95% of her body mass is provided to the young as food (Salomon et al. 2005). These maternal care behaviors lead to a threefold increase in the body mass of
... The nourishment of offspring by the maternal body ('matriphagy') has been described in arachnids and some insects (e.g. Suzuki et al. 2005;Salomon et al. 2011), while foetuses of viviparous caecilian amphibians are known to scrape lipid-rich secretions and cellular materials from their hypertrophied maternal oviducts (e.g. Wake and Dickie 1998). ...
In order to explain the huge variation in parental behaviour, evolutionary biologists have tradition-ally used a cost–benefit approach, which enables them to analyse behavioural traits in terms of the positive and negative effects on the transmission of parental genes to the next generation. Empir-ical evidence supports the presence of a number of different trade-offs between the costs and ben-efits associated with parental care (Stearns 1992; Harshman and Zera 2007), although the mecha-nisms they are governed by are still the object of debate. In fact, Clutton-Brock's (1991) seminal book did not address the mechanistic bases of parental care and most work in this field has been conducted over the last 20 years. Research on mechanisms has revealed that to understand parental care behaviour we need to move away from traditional models based exclusively on currencies of energy or time. Despite repeated claims, the integration of proxi-mate mechanisms into ultimate explanations is cur-rently far from successful (e.g. Barnes and Partridge 2003; McNamara and Houston 2009). In this chapter we aim to describe the most relevant advances in this field. In this chapter, we employ Clutton-Brock's (1991) definitions of the costs and benefits of parental care. Costs imply a reduction in the number of off-spring other than those that are currently receiv-ing care (i.e. parental investment, Trivers 1972), whereas benefits are increased fitness in the off-spring currently being cared for (see also Chapter 1). Benefits may be derived directly from resources allocated to the offspring (e.g. food, temperature), indirectly from protection against predators, or from the modification of the environment in which the offspring are developing (Chapter 1). We begin this chapter by reviewing the traditional idea of resource allocation trade-offs, and also explore how trade-offs need not be based on resources, and the relevance of cost-free resources. We then analyse in more detail studies of the benefits and costs of parental behaviour and, above all, work that combines mechanistic and functional explanations. Finally, we address the control systems that trans-late cues perceived by the organism about costs and benefits allowing individuals to take decisions. 3.2 Trade-offs and the nature of the parental resources
... F. auricularia is a sedentary generalist predator, already present in citrus canopies at the onset of most pest outbreaks, while F. pubescens arrived later to the canopies, but most likely was abundant enough to contribute in the control of citrus pests. Kohno 1997; Kamimura 2003; Matze and Klass 2005; Suzuki et al. 2005) and to evolutionary aspects (Jarvis et al. 2005; Kamimura 2006; Tworzydio et al. 2010). In general, little is known of the ecology of most earwig species. ...
Background/Question/Methods
As omnivorous insects, earwigs are considered key pest predators but they are also occasionally considered pests in agroecosystems. Due to the worldwide distribution of Forficula auricularia L., most published research about earwigs focus on this species. Along with other predators and parasitoids, F.auricularia has been proved to effectively regulate several pest populations in apple and pear trees and vineyards. However, very little is known of the European earwig neither in the Mediterranean region nor in citrus trees. Earwigs and aphids were collected monthly during five years (2006-2010) from citrus canopies using beating trays. Two species of earwigs were found: Forficula auricularia and Forficula pubescens Serville. While the former has been well studied in many aspects, the latter is hardly cited in the literature. The aims of this study were (a) to study the phenology of these two co-occurring species of earwigs in citrus canopies; (b) to examine if the presence of these two species in trees was independent or not; (c) to establish the temporal evolution of their abundance during a five year period, and (d) to evaluate their potential role as pest predators in citrus orchards.
Results/Conclusions
The European earwig in Mediterranean organic citrus trees has two reproduction periods per year; the first period occurs earlier and the second later than what is described in the literature. F. pubescens has only one reproduction period in spring. The presence of these species in citrus trees was independent. In 2006 both species had approximately the same abundance, but during the five years of the study F. pubescens exponentially increased its relative abundance and in 2010 its abundance in canopies relative to that of F. auricularia was 28 times higher. European earwig abundance was negatively related to aphid abundance, suggesting a top-down regulation of aphids by this earwig. By contrast, F. pubescens abundance did not show a significant relationship with aphid abundance. This difference in both species abundance in relation to that of aphids might be explained by the early arrival of F. auricularia in trees (in April) and the later arrival of F. pubescens (in May), when aphid attack was already high. Finally, the observed phenology of the two species of earwigs suggested that they are potential predators of several common citrus pests including aphids, leafminers, woolly whiteflies, and scale insects.
... F. auricularia is a sedentary generalist predator, already present in citrus canopies at the onset of most pest outbreaks, while F. pubescens arrived later to the canopies, but most likely was abundant enough to contribute in the control of citrus pests. Kohno 1997; Kamimura 2003; Matze and Klass 2005; Suzuki et al. 2005) and to evolutionary aspects (Jarvis et al. 2005; Kamimura 2006; Tworzydio et al. 2010). In general, little is known of the ecology of most earwig species. ...
Earwigs are usually considered pest predators in orchards. Because of its worldwide distribution, most research on earwigs focuses on the European earwig Forficula auricularia Linnaeus (Insecta: Dermaptera: Forficulidae). However, very little is known of this species in Mediterranean citrus orchards. Earwigs and aphids were collected monthly during 5 years (2006–2010) from citrus canopies. Two species of earwigs were found: F. auricularia and Forficula pubescens Gené (=Guanchia pubescens), with the latter seldom cited in the literature. The goals of this study were (i) to document the abundance of these two earwig species in Mediterranean citrus canopies; (ii) to determine whether they are positively or negatively associated with each other, or randomly distributed; (iii) to measure the interannual variation of the abundance of both species during a 5-year period and (iv) to evaluate the potential role of earwigs as pest predators in citrus canopies. As compared to colder regions, F. auricularia active period in citrus canopies in our study site lasted longer. Both species co-occurred randomly in canopies. In 2006, both species showed approximately the same abundance, but in 2010, F. pubescens abundance in canopies was 28 times greater than that of F. auricularia. The potential role of earwigs as pest predators is higher in the
Mediterranean than in other colder regions, because of the longer active period. F. auricularia
is a sedentary generalist predator, already present in citrus canopies at the onset of most pest outbreaks, while F. pubescens arrived later to the canopies, but most likely was abundant enough to contribute in the control of citrus pests.
... Actual copulation in earwigs can take several hours and can be repeated before the male and female separate. Suzuki et al. (2005) examined maternal care in Anechura harmandi and found that matriphagy increases the survival rates of nymphs. However, matriphagy and semelparity are the exception in Dermaptera, as many females can have more than one brood if climatic conditions allow. ...
... Direct food provisioning by the mother has been described in F. auricularia (Lamb 1976;Vancassel 1984;Kölliker 2007;Staerkle and Kölliker 2008). Matriphagy, in which offspring feed on their mother, is an extreme form of maternal food provisioning that occurs in Anechura harmandi Burr (Dermaptera: Forficulidae) (Suzuki et al. 2005). Protection from predators is offered by keeping nymphs together and attacking nest invaders. ...
We performed laboratory experiments to study maternal care in Doru lineare Eschs. (Dermaptera: Forficulidae), a predator of the maize pest Spodoptera frugiperda J.E. Smith (Lepidoptera: Noctuidae). Females laid 29.7 ± 8.43 (SD) eggs which took 7–10 days to hatch. Mothers searched for an appropriate nest, where they cleaned and defended eggs and nymphs. Females did not recognize eggs from other females as foreign and adopted them. Other evidence of maternal behavior was also observed, such as egg-cleaning, nest-cleaning, and a lower viability of eggs not cared for by females.
... Alternatively, it may be based on specialized food sources such as milk produced by female mammals (Clutton-Brock 1991), unfertilized trophic eggs as in the poison-arrow frog Dendrobates pumilio (Weygoldt 1980 ), and modified skin produced by females of the caecilian Boulengerula taitanus (Kupfer et al. 2006). The most extreme form of food provisioning is matriphagy, where the hatched offspring consume their mother, as in the spider Diaea ergandros (Evans et al. 1995) and the hump earwig Anechura harmandi (Suzuki et al. 2005). ...
... All earwig (Dermaptera) species studied to date exhibit parental care (Lamb 1976), however, the extent of care varies greatly from species to species (Vancassel 1984). For example, Tagalina papua shows only egg guarding (Matzke and Klass 2005), but the hump earwig, Anechura harmandi, mothers guard and clean the eggs and are killed and eaten by the first-instar nymphs before they disperse from the nest (Kohno 1997; Suzuki et al. 2005). Although nearly 2,000 Dermaptera species have been described (Haas 2003), parental behavior has been examined in only a handful of these species. ...
Provisioning the young is an important form of insect parental care and is believed to improve the survival and growth of the young. Anisolabis maritima Bonelli (Dermaptera: Anisolabididae) is a cosmopolitan species of earwig that shows sub-social behavior in which the females tend clutches of eggs in soil burrows. The defensive and provisioning behaviors of these females were examined in this study. When disturbed, maternal individuals abandoned the nest less than non-maternal individuals. Females brought food to the nest after their eggs hatched, and the survival of the nymphs was increased by provisioning. Even when mothers were removed, providing food to the nymphs increased survival as well as when the nymphs were provisioned by the mother. These results show that A. maritima mothers provision the nymphs and that this provisioning improves their survival.
Haplodiplatyidae is a recently established earwig family with over 40 species representing a single genus, Haplodiplatys Hincks, 1955. The morphology of Haplodiplatyidae has been studied in detail, but its molecular characters remain unclear. In this study, two mitogenomes of Haplodiplatys aotouensis Ma & Chen, 1991, were sequenced based on two samples from Fujian and Jiangxi provinces, respectively. These represent the first mitogenomes for the family Haplodiplatyidae. The next-generation sequencing method and subsequent automatic assembly obtained two mitogenomes. The two mitogenomes of H. aotouensis were generally identical but still exhibit a few sequence differences involving protein-coding genes (PCGs), ribosomal RNA (rRNA) genes, control regions, and intergenic spacers. The typical set of 37 mitochondrial genes was annotated, while many transfer RNA (tRNA) genes were rearranged from their ancestral locations. The calculation of nonsynonymous (Ka) and synonymous (Ks) substitution rates in PCGs indicated the fastest evolving nd4l gene in H. aotouensis. The phylogenetic analyses supported the basal position of Apachyidae but also recovered several controversial clades.
Dermaptera is a relatively small order of free-living insects that typically feed on detritus and other plant material. However, two earwig lineages - Arixeniidae and Hemimeridae -- are epizoic on Cheiromeles bats and Beamys and Cricetomys rats respectively. Both of these epizoic families are comprised of viviparous species. The monophyly of these epizoic lineages and their placement within dermapteran phylogeny has remained unclear. A phylogenetic analyses was performed on a diverse sample of 47 earwig taxa for five loci (18S rDNA, 28S rDNA, COI, Histone 3, and Tubulin Alpha I). Our results support two independent origins of the epizoic lifestyle within Dermaptera, with Hemimeridae and Arixeniidae each derived from a different lineage of Spongiphoridae. Our analyses places Marava, a genus of spongiphorids that includes free-living but viviparous earwigs, as sister group to Arixeniidae, suggesting that viviparity evolved prior to the shift to the epizoic lifestyle. Additionally, our results support the monophyly of Forficulidae and Chelisochidae and the paraphyly of Labiduridae, Pygidicranidae, Spongiphoridae, and Anisolabididae.
I investigated the foragingbehavior of A. ferox females during the reproductive period by presenting the females with 50 mg-cricket nymphs on their webs and comparing the responses across different phases from before egg-laying until matriphagy. The results showed clear variation in the maternal behavior over the period (N= 40 females). Most gravid and incubating females showed active prey-capturing (87 % of gravid females; 72 % of incubating females). Following the eclosion (spiderlings coming out of the eggshell inside the egg sac), however, prey consumption (22 %) declined dramatically, while aggressive responses (menace, attack, kill without consuming) increased (38 %). After trophic egg-laying, the females guarded their young more closely; 45 % of the females did not move, and only 12 % consumed the prey. Eclosion of the spiderlings appeared as an onset of behavioral modification of the mother. Absence of pronounced variation in female body mass after the trophic egg-laying confirmed that they fed very little during the period. A. ferox appears to have evolved the ability to protect its family group against the outside environment at the cost of lost opportunities to gain weight by consuming prey during the post-eclosion period.
Parental care entails physiological costs to the mother. These costs, even if dramatic, are usually reversible and do not result in mortality of the mother. In the spider Stegodyphus lineatus Latreille 1817 (Eresidae), maternal care is extreme and irreversible: mothers regurgitate food for the young and then die when consumed by them (matriphagy). We examined whether the mother's midgut tissues undergo structural changes in preparation for regurgitation and matriphagy. Our histological data show that the midgut diverticula (MD) tissues start to degrade during the egg sac incubation period. When the young emerge from the egg sac, the midgut tissues are partly liquefied and are retained within the MD. The degradation process intensifies when the female feeds her young by regurgitation and liquid tissue is observed within and among the diverticula lobes. The presence of the lumen of a diverticulum during the regurgitation process suggests that degenerated tissues enter the lumen and form the regurgitated fluid. At matriphagy, the abdomen is filled with liquid containing nutritional vacuoles, which the young imbibe after piercing the female's abdomen. We conclude that the MD undergoes a gradual degradation process that maximizes the nutritional potential of the female's body and finally enables complete consumption of her soma. These changes are consistent with the extreme semelparous reproductive system of S. lineatus, where a female invests all of her resources into a single reproductive event. This is the first demonstration of the mechanism underlying suicidal maternal care in an arthropod.
Animals that provide parental care are expected to weigh the value of current offspring against the value of future offspring, such that total investment across all offspring is allocated to maximize lifetime fitness. In this study, we characterize the trade-offs associated with maternal care in the maritime earwig, Anisolabis maritima (Dermaptera: Anisolabididae). We measured the benefits of care in terms of hatching success through removal experiments and the costs of care by comparing the future fecundity of caring females to that of removals. We show that the benefits of care greatly outweigh the costs, providing a seven-fold increase in hatching success. Artificially removed females had larger subsequent clutches and shorter internest intervals, but very low hatching success. Naturally abandoning females always cannibalize all their eggs. Partial clutch cannibalism was a ubiquitous feature of maternal care, although rates were variable among individuals. In post hoc tests, we first addressed the ultimate explanation that filial cannibalism is a way for females to facultatively adjust their investment per clutch in order to maximize future reproduction. We then tested two proximate explanations for filial cannibalism: (1) females that lay more eggs for their given body size tend to consume more eggs, reflecting a nutritional deficiency; (2) females prefer to cannibalize the youngest eggs to reduce the overall duration of egg care. In addition, we consider the alternative explanation that females eat unviable eggs for hygienic reasons. Our results provide support for both energy limitation and hygienic maintenance. Higher rates of egg cannibalism near the very end of nesting were also suggestive of nymphal cannibalism, a phenomenon that will be examined in future work. (c) 2012 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Micromalthus debilis LeConte (1878), has one of the most bizarre life cycles of any metazoan. Reproduction is typically by thelytokous, viviparous, larviform females, but there is also a rare arrhenotokous phase. The active first-instar (triungulin) larva develops into a legless, feeding (cerambycoid) larva. This form either pupates, leading to a diploid adult female, or develops into any of three subsequent types of reproductive paedogenetic forms: (1) a thelytokous female that produces triungulins via viviparity; (2) an arrhenotokous female that produces a single egg that develops into the short-legged (curculionoid) larva, eventually devouring its mother and becoming a haploid adult male; or (3) an amphitokous female that can follow either of the two above reproductive pathways. We speculate that Micromalthus is dependent on maternally transmitted bacteria for the ability to digest rotting wood, and that these bacteria are senescent in males, causing males to be obligately cannibalistic. Obligate male cannibalism, in turn, would have dramatically increased the cost of males, and have created a strong selective advantage for cyclic thelytoky and the other features of the Micromalthus life cycle that minimize the role of the male.
The chapter describes the relationships between phenotypic plasticity through the development and intra- and inter-specific radiation specifically in regard to dermapteran parental behavior. Mainly adults, and specifically, dynamics of their reproductive cycle are concerned. The great majority of studies on behavioral ontogeny concern “higher” animals mainly mammals, where mother-infant relationships imply a type of social bond (psychosocial level) that is not found in insects (biosocial level). This chapter is also guided by the question of behavioral transformations linked with speciation, in particular Darwinian behavioral adaptations arising from the conventional Darwinian mechanism of selection upon genetic variation. It also describes the development of dermapteran parental behavior, then examines this process within the context of intra- and inter-specific adaptive radiation, and lastly, it discusses the theoretical implications of this epigenetic approach.
The possible influences of life history and habitat characteristics on the evolution of semelparity and cannibalism in the
hump earwigAnechura harmandi were studied. This species is univoltine and overwinters as an adult. Females laid single egg-batches during winter in nests
under stones at a riverside in a valley. They took care of the eggs which hatched in early spring and the offspring ate their
mother before dispersing. The valley was sometimes flooded in summer. Nymphs emerged as adults and dispersed to elsewhere
before the rainy season arrived. They returned to the riverside after the rainy season. The flooding and/or summer heat seemed
to be the selective force for the evolution of dispersal behavior and semelparity in this species. The cannibalism of the
female parent by her offspring seemed to have readily evolved after the evolution of semelparity. The unfavorable environmental
conditions seemed to have a large effect on the evolution of semelparity and cannibalism in this species.
Ever since Modeer (1764) first described maternal egg
guarding in the parent bug, Elasmucha grisea,
attempts have been made to understand the evolution of
postzygotic maternal care in insects (Wheeler 1928;
Wilson 1971, 1975; Smith 1980; Zeh & Smith 1985;
Tallamy & Wood 1986; Zeh et al. 1989; Clutton-Brock
1991; Tallamy 1994; Trumbo 1996; Tallamy & Schaefer
1997). The task has been difficult, for the disparate
appearance of this behaviour throughout 13 orders and at
least 45 families of insects has thus far masked evolutionary
patterns. Perhaps the most cited effort is that of
Wilson (1975) who posits four ‘prime movers’ that promote
the evolution of parental care in animals: stable,
structured environments; physically harsh environments;
specialized (scarce, ephemeral, rich or poor) food
resources; and predation. Although they provide an
appealing theoretical framework, these broad categories
lack predictive power because there are myriad examples
of insects, often close relatives of maternal species, that
reproduce under such conditions without the use of
maternal care (Thomas 1995; Trumbo 1996; Tallamy &
Schaefer 1997).
New observations on parental behavior of the earwig, Forficula auricularia L., are reported and the literature on the parental behavior in the Dermaptera is summarized. The construction of the nest, care of the eggs and nymphs, and the duration of parental care are described. The control of parental behavior and the role of the male in nest establishment are also considered.
Subsocial behaviour is the most primitive level of social interaction involving parents and offspring. Life history preadaptations to such behaviour are noted. Conditions that impede survival and development of immatures can promoted subsocial interactions, argued here to be a direct consequence of an association with a particular class of nutritional resource. This resource hypothesis is explored by reference to the principle foods of foliage, wood, detritus, living animals, carrion and dung. Comments are made on maternal vs paternal investment; the former is commoner, but the latter may occur where a male sacrifices future promiscuity for investment into offspring, or where reproduction on a particular resource requires substantial investments in labour and territorial defence. -P.J.Jarvis
The adaptive value of matriphagy, the consumption of the mother by her offspring, in the sub-social spider Amaurobius ferox (Araneae, Amaurobiidae) was experimentally evaluated in terms of the benefits to the offspring and the costs to the mother. Matriphagy resulted in a 2.5-fold weight gain in the offspring over their initial weight, advancement of their moulting time, and larger body mass at dispersal in comparison with clutches deprived of matriphagy, but otherwise well provisioned with prey. Matriphagous offspring were also more successful at capturing large prey items, had a more extended social period, and a higher survival rate at dispersal. Mothers separated from their broods just prior to matriphagy were able to produce second clutches, effectively producing 33% more viable offspring (compared with the first clutches). However, the estimated reproductive outputs of the alternative maternal strategies (being devoted to the first clutch vs. deserting the first and producing a second one) suggest that mothers of A. ferox that are cannibalized by their broods enjoy greater reproductive success than those that escape cannibalism and produce second clutches.
The expression and maintenance of maternal behavior in the earwig,Euborellia annulipes, was examined through manipulation of clutch size, age, and species and through observations of interactions between brooding females. Females underwent discrete gonadotrophic cycles culminating in oviposition of first clutches that were highly variable in size. Neither the head capsule width nor the age of the mother was correlated with clutch size. Maternal care extended through embryogenesis and for the week following hatching. Clutch removal significantly shortened the interclutch interval, indicating that the presence of brood inhibited the onset of the second gonadotrophic cycle. Brooding females readily accepted replacement clutches of the same age. Thus, mothers did not appear to distinguish their own eggs from those of other females. Experimental doubling of clutch size did not significantly reduce the proportion hatching or fledging. In contrast, reducing clutch size diminished the percentage successfully fledging. Manipulation of clutch age resulted in reduced hatching/fledging success. Placing two females, each with newly laid clutches, in the same cage usually resulted in egg transfer from the nest of one female to that of the other within 12 h. Nests of females with larger forceps were significantly more likely to contain both clutches. When mothers with first clutches were paired with mothers with third clutches, eggs were more likely to be transferred to the nest of the older female.E. annulipes females with newly laid clutches appeared to accept as replacement clutches eggs of the earwigDoru taeniatum. Alien clutches were maintained for the typical duration of embryogenesis; however, noD. taeniatum hatchlings were observed.
Young of the Japanese foliage spider, Chiracanthium japonicum, show matriphagy, whereby they consume their own mothers before dispersal. By removing mothers in the laboratory, I examined
the importance of this sacrificial habit for offspring survival and dispersal behavior. Spiderlings that cannibalized their
mothers gained weight more than threefold and dispersed from their breeding nests after molting into the third instar. The
third-instar spiderlings had relatively longer legs than the previous instars and appeared to be more adapted to a solitary
hunting life style. On the other hand, most spiderlings separated from their mothers could not molt into the third instar
and dispersed significantly earlier than those with matriphagy. Furthermore, the lack of matriphagy decreased the survival
rate of predispersal spiderlings. These results showed that matriphagy of C. japonicum has a great advantage in allowing offspring to disperse at a more developed and active instar.
I examined the function of maternal care in a foliage spider,Chiracanthium japonicum. Females of this species make breeding nests with rolled-up grass leaves and provide themselves to spiderlings as food at
the end of maternal care. By removing mothers from their offspring at 2 different times, the effects of maternal care on egg
and spiderling survival rates were estimated separately. Mother attendance greatly improved survival and development of eggs
as well as spiderlings. Detailed observations on the fate of immatures in breeding nests with and without their mothers showed
lower hatching and spiderling emergence rates when mothers were removed. Furthermore, spiderlings that fed on their mother’s
body showed accelerated growth and quickly molted into the 3rd instar with the delay of dispersal. This suggests that matriphagy,
or eating the mother, enables spiderlings of this species to disperse at a later instar. Therefore, I conclude that the maternal
care of this spider consists of guarding offspring, supporting offspring development and feeding spiderlings.
Parental care in earwigs (In Japanese)
- Sasamoto
Peculiar life-cycle of the hump earwig (In Japanese)
- Kohno
Peculiar life-cycle of the hump earwig
- K Kohno
Kohno K (1984) Peculiar life-cycle of the hump earwig (In Japanese).
Iden (Hered) 38:70-75
Parental care in earwigs
- T Sasamoto
Sasamoto T (1978) Parental care in earwigs (In Japanese). Insectarium
15:32-35
The evolution of parental care Making a meal of mother
- Th Clutten-Brock
Clutten-Brock TH (1991) The evolution of parental care. Princeton
University Press, Princeton
Evans TA, Wallis EJ, Elger MA (1995) Making a meal of mother.
Nature 376:299