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Keywords:

  • Benefits;
  • co-adaptation;
  • costs;
  • environment;
  • parental care

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References
  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.

Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References

Parental care is considered a prime example for an altruistic trait that evolved to enhance the fitness of the recipients of care (offspring) at the expense to the donor of care (parents) (Royle et al., 2012). The costs of decreased parental residual reproductive success associated with parental care have to be outweighed by the parents' indirect benefit in terms of an increase in offspring fitness (Hamilton, 1964; Smiseth et al., 2012). This kin-selected indirect fitness benefit to the parents is typically associated with genetic conflicts between parents and offspring over the level of parental investment, because in sexually reproducing species, parents and offspring are genetically not identical (parent–offspring conflict; Trivers, 1974). There has been strong research emphasis on the importance of close genetic relatedness in the evolution of parental care, which resulted in a large number of theoretical and empirical studies (see Alonzo & Klug, 2012). The results of these studies are mixed, probably at least partly because the effect of kinship on the evolution of parental care also depends on variation between individuals and factors affecting the fitness benefits and costs of care, such as ecological conditions, the life history of individuals, conflicts between the sexes, and the social environment in which parents provide care (Alonzo & Klug, 2012).

Wilson (1975) proposed specific hypotheses about how ecological factors may influence the evolution of parental care. He predicted that parental care should predominately evolve under stable structured habitats, unusually stressful physical environments, high predation pressure, and scarce or specialized food sources. It was not until recently that the importance of ecological factors, in relation to the evolutionary origin of parental care, were rigorously investigated in a series of mathematical models. Klug and Bonsall (2010) showed that parental care can evolve from an ancestral state of no care under a range of combinations of ecological conditions and life histories (e.g. egg, juvenile, and adult mortality rates, adult reproductive rate, egg maturation rate, and the duration of the juvenile stage). The authors compared the evolution of parental care in a constant versus a variable environment. They found that in a variable environment, the selection of parental care depends on the interaction between environmental variability, the life-history traits affected by such variability, and the specific costs of care (Bonsall & Klug, 2011). For example, environmental variability reduces selection for parental care when the costs of care are associated with both reduced parental survival and reproductive rate, but favours parental care if the only cost of care is a reduced parental survival rate. Whereas recent theoretical developments support the idea that ecological agents of selection in combination with pre-existing life histories are important, they also revealed that ecological agents on their own are usually not sufficient for the emergence of parental care (Klug & Bonsall, 2010; Klug et al., 2012), leaving scope for other important factors. One of them is the social environment, which results from interactions between the two parents (Smiseth & Moore, 2004), between parents and offspring (Mas et al., 2009) or among siblings (Ohba et al., 2006). Such social interactions are indeed known to shape the benefits/costs ratio of care and, hence, possibly to influence the strength of natural selection on parental care once a basic level of care has evolved (Royle et al., 2002; Smiseth et al., 2012).

Our general aim in this review is to summarize and discuss hypotheses and empirical evidence from insects regarding influences of ecology, life history, and the social environments on the evolution of parental care. A great diversity in the forms of parental care has been reported across taxa (Tallamy & Wood, 1986; Clutton-Brock, 1991; see Royle et al., 2012 for a recent review). Besides birds and mammals, insects are a promising, albeit often understudied, system to investigate the evolution of parental care because it presents a particularly wide diversity in the forms, duration, and intensity of care (Trumbo, 2012) (see Fig. 1 for examples). Table 1 illustrates several well-studied examples of the variety of forms of parental care in non-eusocial insects and gives information about the sex of the caregiver.

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Figure 1. A selection of insect species that provide parental care. (a) A female burrower bug (Sehirus cinctus) provisioning mint nutlets to her offspring (photograph: Patrick Alexander). (b) A female European beewolf (Philanthus triangulum) carrying a paralysed honeybee in flight to her nest (photograph: Gudrun Herzner). (c) A female of the European earwig (Forficula auricularia) with her first-instar nymphs (photograph: Joël Meunier). (d) A burying beetle Nicrophorus vespilloides providing food to its larvae via regurgitation (photograph: Per Smiseth). (e) Fourth-instar nymphs of the wood-feeding cockroach Salganea taiwanensis feeding on the stomodeal fluids of the female (view from below) (photograph: Kiyoto Maekawa). (f) A female treehopper (Platycotis vittata) with her brood of fourth- and fifth-instar offspring (photograph: Jennifer Hamel).

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Table 1. Forms of parental care in insects. This table show a summary of well-studied and taxonomically diverse examples in which the benefits of parental care have been shown. Blank cells represent missing information
Order/Family/speciesCare giver Form of parental careReferences
  1. B = biparental; EA = egg attendance; EB = egg brooding; F = female; FP = food provisioning, FP1 = mass provisioning, FP2 = progressive provisioning, FP3 = matriphagy; M = male; NI = care after nutritional independence; OA = offspring attendance; OB = offspring brooding; V = viviparity.

BLATTODEA
Blaberidae
Blaberus craniiferF EB     Nalepa & Bell (1997)
Byrsotria fumigataF EB     Nalepa & Bell (1997)
Diploptera punctataF  V    Roth & Willis (1957) Nalepa & Bell (1997)
Geoscapheus spp.F EB     Nalepa & Bell (1997)
Lanxoblatta emarginataF   OA   van Baaren et al. (2003)
Macropanesthia spp.F EB     Nalepa & Bell (1997)
Nauphoeta cineraF EB     Nalepa & Bell (1997)
Neogeoscapheus spp.F EB     Nalepa & Bell (1997)
Parapanesthia spp.F EB     Nalepa & Bell (1997)
Perisphaerus spp.F    OB  Roth (1981)
Phortioeca nimbataF   OA   van Baaren et al. (2003)
Rhyparobia maderaeF EB     Nalepa & Bell (1997)
Salganea spp.B   OA FP2 Nalepa & Bell (1997); Maekawa et al. (2008)
Salganea taiwanensisB     FP2 Maekawa et al. (2008)
Schultesia lampyridiformisF   OA   van Baaren et al. (2003)
Thanatophyllum akinetumF   OA   Nalepa & Bell (1997); van Baaren et al. (2003)
Thorax porcellanaF    OB  Nalepa & Bell (1997)
Blattellidae         
Blattella germanicaF EB     Roth & Willis (1957); Nalepa & Bell (1997)
Blattella vagaF EB     Roth & Willis (1957); Nalepa & Bell (1997)
Cryptoceridae         
Cryptocercus kyebangensisB   OA FP2 Park et al. (2002)
Cryptocercus punctulatusB   OA FP2NISeelinger & Seelinger (1983); Nalepa (1990)
Cryptocercus spp.BEA  OA FP2 Nalepa & Bell (1997); Maekawa et al. (2008)
COLEOPTERA
Curculionidae
Monarthrum spp.F   OA FP1 Kirkendall et al. (1997)
Trypodendron lineatumF   OA   Kirkendall et al. (1997)
Xyleborus spp.FEA  OA FP Kirkendall et al. (1997)
Passalidae         
All speciesB   OA FP2 Schuster & Schuster (1997)
Scarabaeidae         
Onthophagus taurusF     FP1 Moczek (1998)
Silphidae         
Nicrophorus spp.B   OA FP2 Scott (1990); Trumbo (1990)
Ptomascopus morioF   OA   Trumbo et al. (2001); Suzuki & Nagano (2006)
Staphylinidae         
Bledius spectabilisFEA  OA FP2 Wyatt (1986)
DERMAPTERA
Anisolabididae
Anisolabis maritimaFEA  OA FP2 Bennett (1904); Suzuki (2010)
Euborellia annulipesFEA  OA FP2 Rankin et al. (1995)
Euborellia plebejaFEA      Kamimura (2003)
Forficulidae         
Anechura bipunctataFEA  OA   Vancassel (1984)
Anechura harmandiFEA  OA FP3 Kohno (1997); Suzuki et al. (2005)
Forficula auriculariaFEA  OA FP2 Weyrauch (1927); Lamb (1976a); Staerkle & Kölliker (2008)
Forficula decipiensFEA  OA   (M. Kölliker, unpublished)
Forficula lesneiFEA  OA FP2 Timmins (1995)
Labiduridae         
Labidura ripariaFEA  OA FP2 Radl & Linsenmair (1991)
Spongiphoridae         
Chaetospania borneensisF  V    Kocarek (2009)
Pygidicranidae         
Tagalina papuaFEA  OA   Matzke & Klass (2005)
EMBIOPTERA
Anisembiidae
Anisembia texanaFEA  OA   Choe (1994); Edgerly (1997)
Clothodidae         
Antiluparia urichiFEA  OA   Edgerly (1997)
Oligotomidae         
Oligotoma humbertianaFEA      Edgerly (1997)
HEMIPTERA
Acanthosomatidae
Elasmucha ferrugataFEA  OA   Kaitala & Mappes (1997)
Elasmucha fieberiFEA  OA   Melber & Schmidt (1975); Kaitala & Mappes (1997)
Elasmucha griseaFEA  OA   Melber & Schmidt (1975); Kaitala & Mappes (1997)
Belostomatidae         
All sp BelostomatinaeM EB     Smith (1997); Estévez & Ribeiro (2011)
All sp LethocerinaeMEA      Smith (1997); Estévez & Ribeiro (2011)
Cydnidae         
Adomerus triguttulusFEA  OA FP2 Nakahira (1994)
Canthophorus niveimarginatusFEA    FP2 Filippi et al. (2008)
Parastrachia japonensisFEA  OA FP2 Filippi-Tsukamoto et al. (1995b); Hironaka et al. (2005)
Sehirus cinctusFEA  OA FP2 Sites & McPherson (1982); Kight (1997)
Membracidae         
Polyglypta disparFEA  OA   Eberhard (1986)
Publilia concavaFEA  OA   Bristow (1983); Zink (2003b, 2005)
Publilia reticulataFEA  OA   Bristow (1983)
Pyrgauchenia tristaniopsisFEA      Stegmann & Linsenmair (2002)
Umbonia crassicornisF   OA   Cocroft (1996)
Reduviidae         
Rhinocoris carmelitaFEA      Thomas & Manica (2005)
Rhinocoris tristisM/FEA      Beal & Tallamy (2006)
Tingidae         
Gargaphia solaniFEA  OA   Tallamy & Denno (1981)
Leptobyrsa decoraFEA  OA   Loeb & Bell (2006)
HYMENOPTERA
Bethylidae
Goniozus nephantidisFEA  OA   Hardy & Blackburn (1991)
Megachilidae         
Osmia lignariaF     FP1 Torchio & Tepedino (1980)
Sphecidae         
Ammophila aureonotataF     FP1 Evans (1959)
Ammophila hartiF     FP2 Evans (1959)
Ammophila junceaF     FP1 Evans (1959)
Ammophila nigricansF     FP1 Evans (1959)
Ammophila placidaF     FP1 Evans (1959)
Ammophila proceraF     FP1 Evans (1959)
Ammophila pubescensF     FP2 Evans (1959); Field & Brace (2004)
Ammophila sabulosaF     FP1 Field (1989)
Philanthus triangulumF     FP1 Strohm & Linsenmair (2001); Herzner & Strohm (2007)
ORTHOPTERA
Gryllidae
Anurogryllus muticusFEA  OA FP2 West & Alexander (1963)

Our review starts by discussing the empirical support for different ecological factors that favour the emergence of parental care. We pay particular attention to how ecological factors may interact with animal life histories (in particular semelparity versus iteroparity) and conclude that it remains unclear whether life histories are evolutionary causes or effects of parental care (or a combination of the two). We then elaborate on how the social environment can influence parental care via interactions within and between families. We discuss how family interactions can affect potential benefits and costs associated with parental care, and how parent and offspring strategies may evolve as a consequence of these socially mediated modifications of selection on parents and offspring. Finally, we discuss our perspective on areas of further research into the evolution of parental care and conclude that insects, with their broad diversity in extent and forms of care, offer a unique opportunity to conduct this kind of research.

Throughout this review, we follow the definition of parental care by Royle et al. (2012) 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’. Because we are interested in parental care per se, we decided to not include eusocial insects (e.g. Isoptera, Hymenoptera) in this review, because maternal care (i.e. from the queen to the brood) is commonly expressed only relatively briefly during colony foundation (Bourke & Franks, 1995; Queller & Strassmann, 1998; Boomsma, 2009). We limit our discussion to the evolution of parental care per se without addressing why it was often female uniparental care, instead of male uniparental or biparental care, that evolved. We correspondingly provide examples from these different modes of care without discussing selection on male versus female parental care, which was previously discussed, for example, in Tallamy (2001) and Trumbo (2012). For excellent former reviews on parental care in invertebrates (including insects as well) and on general social living in non-eusocial insects, we refer the interested reader to Trumbo (2012); Tallamy & Wood (1986) and Costa (2006), respectively.

Ecology, life history and insect parental care

  1. Top of page
  2. Abstract
  3. Introduction
  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References

In the following section we will explore previously proposed hypotheses for how ecological factors and variation in life history shape the evolution of parental care in insects. To this end, we first describe how ecological agents of selection are theoretically related to different forms of care, as hypothesized by Wilson (1971, 1975) and illustrate the evidence and its limits across insect taxa. Although the different ecological factors, in reality, probably rarely operate in isolation, we discuss them as separate, albeit not mutually exclusive, hypotheses for ecological factors that favour the evolution of parental care (Wilson, 1975).

Do harsh environmental conditions drive the evolution of insect parental care?

Whereas adaptations increasing egg development under harsh environmental conditions, such as heat stress, desiccation or high humidity, may include protection of the eggs themselves (e.g. a resistant egg shell), parental egg attendance provides an alternative route for resisting these factors. Attendance is expected to be superior to direct adaptations by the eggs if the parent suffers substantially less from the challenging condition than the eggs and/or the cost of the protective adaptation is higher than the cost of attendance for parents (i.e. the costs of egg attendance to the parents are exceeded by the benefits to the eggs). An added benefit of adaptation through parental care is that a caring parent can flexibly adjust its caring behaviour when necessary, whereas a resistant egg shell would be a fixed trait (see, e.g. Field & Brace, 2004).

Several studies provide direct or indirect empirical support for this hypothesis by reporting the benefits of maternal care under specific physical environmental constraints. For example, females of the terrestrial staphylinid beetle Bledius spectabilis live in the inhospitable habitat of the intertidal saltmarsh, wherein their burrows experience daily floods by the tide (Wyatt, 1986). To prevent flooding of their nest and anoxia of their eggs, females provide care in the form of closing the entrance of their burrow during high tide and reopening it at low tide (the latter being vital for respiration in the anaerobic soil). In the shield bug Parastrachia japonensis or the European earwig (Forficula auricularia), females attend their eggs and move them to a new nest site, if the physical conditions become unfavourable due to flood or desiccation (Weyrauch, 1927; Filippi-Tsukamoto et al., 1995a). Male belostomatid water bugs like Belostoma flumineum engage in brooding behaviour by keeping eggs wet, frequently exposing them to atmospheric air, and maintaining an intermittent flow of water over them by stroking them with the hind legs (Smith, 1976; Estévez & Ribeiro, 2011). If eggs become detached from the males, they fail to hatch. 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. 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. For instance, the brood sac of lecithotrophic and matrotrophic viviparous cockroaches such as Rhyparobia maderae or Diploptera punctata protects the developing offspring from heat, cold, moisture, desiccation, anoxia, and osmotic stress within the female body (Nalepa & Bell, 1997).

In these examples, it seems likely that harsh environments contributed to the described parental adaptations. Nevertheless, harsh conditions do not necessarily favour the evolution of parental care, because not only do they usually increase the potential benefits of parental care to offspring, but they may also induce parent–offspring competition for limited resources or enhance the costs to the parents to provide care under such aggravated conditions. Irrespective of the type of ecological harshness, it generally holds that if the costs of care exceed the associated benefits, care will not be selected for despite the potentially large benefits for the offspring (Clutton-Brock, 1991; Royle et al., 2012). Based on available data, it is currently difficult to judge whether the limited support is due to the limited cases in which parental care actually evolved under such conditions (providing evidence against evolution of parental care under harsh conditions), or to the limited amount of systematic research. Even if identified, a phylogenetic association between parental care and harsh environments does not prove that parental care evolved in response to selection imposed by such environments. Instead, such an association may reflect that species that have evolved parental care for some reason unrelated to the harshness of the environment may be able to colonize habitats that otherwise would be inhospitable to ancestral species without parental care. There is clearly a need for further research on the question of if, and how, harsh environmental conditions favour the evolution of parental care, which should involve a combination of phylogenetic analyses and manipulative experiments to test directly how environmental harshness affects selection on parental care (i.e. using fitness assays under different environments with and without care).

Do ephemeral or distant food sources and specialized foraging drive the evolution of insect parental care?

Parental care is expected to allow the offspring to obtain food resources indirectly through the provisioning parent when food sources are ephemeral and occur clumped in space or time, or if they are difficult to access or process (as is often the case in specialized foraging). A critical problem when offspring need access to ephemeral and rare food sources is the extent to which a suitable and safe site for the offspring (e.g. a burrow or nest) is spatially disconnected from the food sources required for energy uptake. If juveniles are less mobile than adults, a provisioning parent may be able to provide both sufficient food and safe shelter at sustainable cost, selecting for parental provisioning of the ephemeral food source. The co-evolution of parental food provisioning and egg/offspring attendance for protection against natural enemies was recently modelled by Gardner and Smiseth (2011). In this model, parental food provisioning evolved from offspring attendance only if parental food provisioning was more efficient than offspring self-feeding, which is more likely to apply when food resources are ephemeral or difficult to access or process. Therefore, the model is in line with the general argument that these environmental factors may be important for the evolution of food provisioning.

There are well-studied examples of food provisioning among insects where the species feed on ephemeral food sources and/or where the offspring are spatially disconnected from it. For example, females of the shield bug P. japonensis provision nymph-containing nests progressively with drupes of a single host tree, Schoepfia jasminodora (Olacaceae), distant from the nest (Filippi et al., 2000). Similarly in the burrower bug Sehirus cinctus, nymphs only eat seeds of a few plant species, in particular Prunella vulgaris (Labiaceae) and Lamium purpureum (Labiaceae), which are available for only a few weeks each spring, and mothers might be better in competing for this limited resource (Kight, 1997).

The cockroach Cryptocercus punctulatus is an example of a species where specialization for a food source may underlie the evolution of parental care. In this wood-feeding species, nymphs are not able to directly process wood. First- and second-instar nymphs feed on hindgut fluids of both parents. Such behaviour allows them to acquire endosymbionts (intestinal flagellata), which are necessary for cellulose digestion and, hence, for the maintenance of this specialized foraging behaviour (Seelinger & Seelinger, 1983; Nalepa & Bell, 1997). In wood-feeding passalid beetles, all stages must feed on the faeces of mature adults. Faeces comprise shredded, digested wood, inoculated with bacteria and fungi from the adult digestive tract (Schuster & Schuster, 1997). Both Cryptocercus cockroaches and Passalid beetles feed on specialized food sources, but it should be noted that they also inhabit rather stable and structured environments (inside deadwood), another ecological factor that was hypothesized to promote the evolution of parental care (see later). It seems likely that a combination of these two factors was ultimately responsible for the evolution of parental care in these species.

In some species, females produce trophic eggs, i.e. unfertilized eggs that are used by hatched offspring as food sources – as, for example, in the Hemipteran Adomerus triguttulus (Kudô & Nakahira, 2004). We refer the interested reader to Trumbo (2012) for a more detailed discussion of this form of care.

Food provisioning is also present in species with non-specialized foragers feeding on non-ephemeral food sources. For instance, the European earwig, F. auricularia, is omnivorous and offspring are only partly disconnected from the food source, since nymphs are able to self-forage independently from an early age (Lamb, 1976a,1976b; Kölliker & Vancassel, 2007). Still, female food provisioning occurs across the order Dermaptera (Costa, 2006).

Given the inconclusive qualitative evidence, the hypothesis that ephemeral food sources and specialized foraging enhance the evolution of parental care would need a full quantitative test. Such tests should take into account other ecological conditions experienced by the species, its life history, the nesting habit and the feeding habit of the species, because selection for parental care is most likely under the combined influences of multiple factors (i.e. survival costs; Bonsall & Klug, 2011; Trumbo, 2012), for example when safe nests cannot be built close to the food source (Gardner & Smiseth, 2011), and/or when the offspring survival without parental assistance (mainly pre-digestion) is low.

Do natural enemies (predators, parasitoids, parasites, microbes) drive the evolution of insect parental care?

Predation was suggested repeatedly to play an important role in the evolution of parental care (Wilson, 1975; Tallamy & Denno, 1981). Whereas this hypothesis was originally put forward with regard to predators, it also applies in principle to any other natural enemy that can specifically impose harm upon offspring, such as parasitoids (Field & Brace, 2004) or microbes competing with offspring for food resources (Rozen et al., 2008; see Trumbo, 2012 for a detailed discussion). Exposure to natural enemies, especially of eggs and juveniles, may select for parental care only if the parents suffer substantially less from their exposure than the offspring. Protection can occur through egg/offspring attendance but other protective adaptations, such as the ovipositor or the resistant egg shell, can provide alternatives to enhance offspring fitness under pressure from natural enemies (Zeh et al., 1989).

The benefits of maternal egg/offspring attendance on offspring survival have been broadly studied and received consistent empirical support across insect species. For example, in the shield bug genus Elasmucha, females shelter the eggs and nymphs by covering them with their body and fanning their wings when attacked. Egg survival was reported to be very low without care (Melber & Schmidt, 1975; Kaitala & Mappes, 1997), mostly due to predation. Females of the lace bug Gargaphia solani also show maternal antipredator behaviour and remain with their progeny throughout all five nymphal instars (Tallamy & Denno, 1981). In the absence of predators, nymphs suffer no ill effects if raised without their mother, but when nymphs were experimentally orphaned under normal field conditions, only very low numbers survived to maturity due to predation (Tallamy & Denno, 1981). Such effects have also been described in a sister species, Gargaphia tiliae (Hardin & Tallamy, 1992). In the staphylinid beetle B. spectabilis, maternal egg and offspring attendance protects eggs and larvae from predatory beetles or parasitoid wasps (Wyatt & Foster, 1989a,1989b). In the treehopper Publilia concava, maternal egg attendance effectively keeps away predators and the eggs are substantially more susceptible to these predators than are adults. Females exhibit two alternative tactics: immediate abandonment after oviposition or egg attendance until and beyond hatching. Zink (2003a) showed that a female attending her eggs until hatching doubled her hatching success relative to a female that abandoned her eggs immediately after laying. However, in terms of lifetime reproductive success, the enhanced fitness of the tending females through higher offspring survival was balanced by the reduced lifetime number and size of their clutches. Thus, tending and non-tending females had roughly similar fitness, which could explain why the two alternative reproductive tactics are maintained in treehopper populations (Zink, 2003a).

These are examples for interspecific predation. But intraspecific predation (i.e. cannibalism) can also be an important agent of selection in predatory insect species. As an example, a recent study in the earwig Anisolabis maritima demonstrated experimentally that egg attendance by females protects the eggs from being cannibalized by conspecifics (Miller et al., 2011).

Field and Brace (2004) showed experimentally in Ammophila wasps how progressive provisioning females can significantly reduce the impact of parasitism by cuckoo flies (Diptera: Miltogramminae), a major natural enemy of wasps. The cuckoo flies deposit live maggots that kill the immature wasp and then eat the provisions. Only wasp mothers of the progressively provisioning species could intervene and remove the fly maggots, which was not possible for mothers of mass provisioning species. Thus, there was an added benefit of progressive provisioning beyond the provided food in terms of protection against a parasite.

Empirical support for the benefits of parental care against competing microbes has been found in several species. Infestation by microorganisms is known to decrease offspring fitness either by killing the larvae or by decreasing progeny size and reproductive success. In the European beewolf (Philanthus triangulum), females provision brood cells with paralysed honeybees as larval food. Because the brood is located in warm and humid cells, there is a high risk of microbial decomposition of the provisioned food. Preservation of prey is achieved by the maternal application of chemical secretions that reduce fungal growth (Strohm & Linsenmair, 2001; Herzner & Strohm, 2007). An analogous mechanism was recently described in the burying beetle Nicrophorus vespilloides, where parents obligatorily breed on carcasses of small vertebrates, and larvae face intense competition with microbes over the carcass. The study by Rozen et al. (2008) showed that parents apply substances (e.g. lysozyme) that inhibit microbial growth and, hence, protect offspring by limiting the development of microbes that would otherwise quickly degrade the quality of the food source. The study further showed that the parental antimicrobial care resulted in higher larval body mass and survival. In the European earwig (F. auricularia), females have been shown to groom their clutch of eggs, a behaviour that has been hypothesized to prevent fungal infections and the moulding of eggs in their underground nests (Weyrauch, 1927; Lamb, 1976a).

Overall, the evidence seems robust for benefits of parental care in species where offspring face high risks of suffering fitness losses due to natural enemies that specifically target offspring or the resources they need for development and survival. Whether the pressure exerted by natural enemies is sufficient to favour the emergence of parental care remains to be confirmed experimentally, for instance by following changes in the level of parental investment in families reared under high and low predation pressures (i.e. experimental evolution). Furthermore, studies could also compare the effect of egg- or juvenile-specific predators with that of general predators, which differentially affect the cost/benefit ratio of protection to the parents and therefore the strength of selection on pre- and postnatal care.

Do predictable environments and life-history variation drive the evolution of insect parental care?

The reason why stable predictable environments may favour the evolution of parental care is linked with life-history evolution. Wilson (1975) and Tallamy and Brown (1999) suggested two contrasting hypotheses regarding the evolution of parental care and the mode of parity. Wilson (1975) argued that when a species adapts to stable, predictable environments, K-selection for an iteroparous life history (i.e. multiple reproductive attempts) tends to prevail over r-selection for a semelparous life history (i.e. single reproductive attempt). Under K-selection, individuals are predicted to live longer and grow larger, and also to produce a smaller number of offspring over multiple reproductive attempts, each with a high reproductive value and correspondingly high levels of parental investment. Following this line of argumentation, parental care is expected to predominately evolve among iteroparous species due to the high expected fitness returns on parental investment when each offspring represents a substantial fraction of lifetime reproductive success (here referred to as ‘iteroparity hypothesis’). Tallamy and Brown's (1999) alternative hypothesis makes the opposite prediction that parental care should evolve more readily in semelparous species, because of the low evolutionary cost of care to parents in terms of residual fitness. Under this hypothesis, iteroparous insects should provide either no parental care or less care than related semelparous species. The ‘iteroparity’ and ‘semelparity’ hypotheses suggest that the emergence of parental care does not primarily result from ecological selection pressures, but instead from life-history pre-adaptations shaping the investment trade-off between current and future reproduction.

Qualitative comparisons have been carried out to test these two hypotheses with mixed results. Some studies provide support for the ‘semelparity hypothesis’. For example, Stegmann and Linsenmair (2002) tested this hypothesis in the membracid Pyrgauchenia tristaniopsis. Here, females exhibit relatively basic forms of care (i.e. egg attendance only) associated with a moderate degree of iteroparity (37% females produced a second clutch), whereas other membracid species generally express more elaborate forms of maternal care (i.e. egg and offspring attendance) and are typically semelparous. The authors interpreted this result as consistent with the ‘semelparity hypothesis’, in that iteroparity was associated with lower levels of maternal care. In another study, Nagano and Suzuki (2008) compared maternal investment in future reproduction between two species of Nicrophorine beetles: Nicrophorus quadripunctatus, which displays more elaborate parental care (carcass preparation, offspring attendance and provisioning); and Ptomascopus morio, which displays simpler parental care (offspring attendance only). In contrast to predictions of the ‘semelparity hypothesis’, the authors found that Nicrophorus quadripunctatus can oviposit several times in one breeding season and that they regulate their clutch size more strictly than P. morio. For more conclusive comparative tests, studies are now needed that relate parental care to parity across more than two species. Any two compared species are likely to differ in many ways that may also affect parental care (e.g. also ecology), which may confound the relationship and mask present patterns. Provided adaptive associations between life history and parental care exist, a different approach to test these hypotheses can be the comparison within species or within populations between individuals with different parity. Meunier et al. (2012) tested the association between the levels of maternal care and second clutch production in a population of the European earwig, F. auricularia, where semelparous and iteroparous females coexist. Contrary to the ‘semelparity hypothesis’, their results showed that iteroparous females provided significantly higher levels of maternal care in terms of food provisioning. They also produced larger first clutches and a larger total number of eggs (first and second clutch combined) than semelparous ones. The study suggests that the intrinsic condition of earwig females plays a key role in the level of maternal care and investment in future reproduction, in that high-condition females can afford both being iteroparous and providing more care despite a likely underlying trade-off between current and future reproduction.

One potential reason for the mixed evidence for an association between mode of parity and parental care is that the distinction between evolutionary cause and effect of parental care in terms of life history remains ambiguous. Is maternal care the consequence of a semelparous life history (as suggested by the ‘semelparity hypothesis’), or is semelparity the consequence of the costs of parental care (referred to as the ‘cost-of-care hypothesis’)? Both directions of effects are likely to occur at differing relative strength between species. The question of whether a particular parity is a life-history pre-adaptation favouring the evolution of parental care, or whether it is, instead, the consequence of evolved parental care and the associated costs in terms of parental residual reproductive value has, to our knowledge, not yet been tackled theoretically or empirically. This distinction could be resolved through comparative phylogenetic studies by reconstructing the ancestral state and following the gain and loss of parental care in association with changes in parity. In Fig. 2 we provide the three phylogenetic hypotheses for the evolutionary association of parental care and mode of parity in insects and explain the different possible scenarios.

image

Figure 2. Phylogenetic hypotheses for the evolutionary association of parental care and mode of parity in insects. In each panel (a)–(c), the ancestral state is depicted to the left of the tree, and the predicted derived states under each hypothesis to the right of the tree. (a) Wilson's ‘iteroparity hypothesis’ (1975): Wilson's hypothesis would be supported if care evolves in an iteroparous species as novelty from a semelparous ancestor, and no care remains associated with semelparity. (b) Tallamy and Brown's ‘semelparity hypothesis’ (1999): The ‘semelparity hypothesis’ would be supported if care evolved in a semelparous ancestor without care and iteroparous species derived from the same ancestor show no care. (c) The ‘cost of care hypothesis’: The hypothesis that semelparity is the consequence of a cost of care would be supported if care evolved in an iteroparous ancestor without care resulting in lineages where maternal care and semelparity co-occur as evolutionarily derived states.

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To conclude, despite a wealth of descriptions of diverse forms of parental care across insect species that vary in life history and inhabit different ecological niches, only little research has directly tested how environmental factors and life-history variation affect the benefits and costs of care (see also Trumbo, 2012). As previously mentioned, more experimental studies are needed, as well as phylogenetic analyses that combine the potential effects of a species ecology and life history on the evolution of parental care. Such an approach would provide a clearer picture of the importance of each ecological factor in relation to the evolution of parental care, while correcting for phylogeny and taxon biases resulting from differences in research effort across taxa, (e.g. the broadly studied cockroaches; see Table 1). To this end, some of the ecological parameters require standardized definitions (e.g. ephemeral food sources or harsh environments) and ways of measurement, in particular if we aim at comparative tests between insect taxa.

Social environment and the evolution of insect parental care

  1. Top of page
  2. Abstract
  3. Introduction
  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References

Parental care is typically associated with social interactions, such as those between parents and offspring or among siblings. The transition from solitary to group (family) living entails the emergence of a novel – social – environment that is characterized by the aggregation of parents and offspring, the resources provided by parents and the ensuing intensified social interactions among family members. This social environment forms part of an individual's ecology and generates new selection pressures, for example through selection on the effective transfer and usage of parentally provided resources, or through conflicts of interest within and between families (Trivers, 1974). Caring parents are a social environment to which offspring should adapt, and offspring are a social environment to which parents should adapt, and these novel selection pressures should lead to parent and offspring adaptations to family life and the co-adaptation of their traits (Kölliker et al., 2012).

When studying how the social environment influences costs and benefits of parental care, we have to consistently partition fitness components between parents and offspring (Wolf & Wade, 2001; see Smiseth et al., 2012 for a review). Parental care is beneficial to the offspring because it increases their direct fitness. From the perspective of the parent (or a parental care gene), the offspring fitness benefit is an indirect fitness benefit because the fitness of the genetically related recipient of care (i.e. the offspring) is enhanced, not that of the donor of care (i.e. the parent). Similarly, parents may pay a direct fitness cost of care in terms of their fecundity. From the perspective of the offspring, the parental fitness costs are indirect costs, because they are paid by genetically related individuals (i.e. the parents). These benefits to offspring and costs to parents lead to genetic conflicts over parental care (Trivers, 1974). It is expected that this selection favours mechanisms that contribute to a resolution of family conflicts, for example through the evolution of parent–offspring communication (reviewed in Kilner & Hinde, 2012). In insects, offspring influences on parental care have been shown to include vibrational signals (e.g. in treehoppers; Cocroft, 1996, 2001), tactile and visual begging (e.g. in the burying beetle N. vespilloides; Smiseth et al., 2003) and chemical signalling, that is solicitation pheromones (e.g. in the burrower bug S. cinctus and the earwig F. auricularia; Kölliker et al., 2006; Mas et al., 2009; Mas & Kölliker, 2011; see Mas & Kölliker, 2008 for review).

The reciprocal nature of parents and offspring influencing each other's fitness leads to selection on particular combinations of parental care and offspring traits, favouring co-adapted parent and offspring strategies. Co-adaptation models make two main predictions: first, that there is a genetic or epigenetic correlation between the levels of offspring demand and parental supply and, second, that a mismatch between parental and offspring strategies comes at a cost to family members (reviewed in Kölliker et al., 2012). Whereas these predictions were tested across numerous bird and mammalian species, parent–offspring co-adaptation has been explored in only three insect species so far. The first prediction of co-adaptation models was tested in the burrower bug S. cinctus and the burying beetle N. vespilloides using cross-fostering experiments, both providing evidence of a genetic correlation between maternal food provisioning and offspring begging (Agrawal et al., 2001; Lock et al., 2004). The second prediction of co-adaptation models was tested in N. vespilloides and in the European earwig F. auricularia. In N. vespilloides, offspring reared by foster females, i.e. in families with mismatched parental and offspring strategies, survived significantly less well than offspring reared by their own mother (Lock et al., 2004), and a recent study in F. auricularia demonstrated that earwig mothers caring for offspring with experimentally mismatched strategies suffered from fitness costs in terms of future reproduction (Meunier & Kölliker, 2012a).

Social environment and the costs of parental care

When multiple parents are breeding in close proximity, the potential network of social interactions is expanded beyond the core family (parents and offspring). Parents might interact with their own offspring, but also with other parents and their offspring. Such between-family interactions can be beneficial (in case of cooperative behaviours) or costly (in case of local competition for resources or brood parasitism). If the fitness or productivity of all individuals involved is increased simultaneously, we find a cooperative outcome due to direct benefits of communal breeding or brood mixing (Lin & Michener, 1972). Brood mixing can occur in species where offspring are mobile and can join other families. However, if an individual's expected reproductive output is even slightly decreased by the invading individual, the invader is more appropriately termed a parasite (Eberhard, 1986). In brood parasitism, one individual exploits the parental care invested by another individual. This could be through the female in case of egg dumping or through the offspring in case of brood mixing. Brood parasitic strategies are predicted to evolve, for example, when breeding sites are in close proximity and there is an opportunity for parental care to be misdirected. As a result, selection should favour kin recognition and guarding strategies in order for caring parents to avoid investment in foreign offspring, and offspring strategies to overcome such defense mechanisms in parents (reviewed in Keller, 1997).

Intraspecific brood parasitism was described in a number of insect species; for example, in the dung beetle Onthophagus taurus (Moczek & Cochrane, 2006), females use cow or horse dung to form brood balls that also serve as a food source for the larvae. Each brood ball contains a hollow chamber holding one egg. Females only oviposit one egg per brood ball, which constitutes the sole amount of food available for larvae to complete larval development (Moczek, 1998). Egg dumping occurs as brood parasitic females were reported to replace conspecific eggs inside brood balls produced by another female with their own egg (Moczek & Cochrane, 2006). The authors suggested that the refilling of tunnels with previously excavated soil or sand by the caring parents is an adaptation to limit parasitism by conspecific females that makes it more difficult for other females to locate brood balls underground.

Parasitic strategies can also include social parasitism through the dispersal of mobile offspring invading foreign family groups. In the burrower bug S. cinctus, oviposition sites are aggregated in the field (Agrawal et al., 2004). The authors could not find evidence that neighbouring females were closely related, so brood mixing events could not have contributed to the females' inclusive fitness. Agrawal et al. reported that brood mixing occurred frequently in experimental studies, mainly initiated by nymphs under limited food supply. This could suggest that, under restricted food conditions, nymphs change their strategy from remaining with their own mother to dispersing and exploiting care from unrelated females, which could reflect brood parasitism. A field study by Kölliker and Vancassel (2007) showed that offspring of the European earwig F. auricularia dispersed from their own burrow and joined foreign family groups, and that this dispersal occurred more readily when the mother was removed (see also Kölliker, 2007).

In the case of intraspecific brood parasitism, conspecifics provide the only hosts for brood parasites and obligate parasitism cannot become fixed in a population. De Valpine and Eadie (2008) suggested that the advantages of egg dumping are likely to be greatest when the frequency of parasitism is low and many host nests are available containing few parasitic eggs. Thus, the parasitic strategy is expected to evolve under negative frequency-dependent selection, and the advantages will decrease as the frequency of parasitism increases and more host nests contain many parasitic eggs. As already pointed out by Müller et al. (1990), so far, we are unaware of cases of intraspecific brood parasitism in which individuals are restricted to either exclusive parasitic or non-parasitic behaviour. Intraspecific brood parasitism seems, rather, to be affected by environmental conditions such as population density (see the section on ‘Ecological influences on social interactions’ below) or the low likelihood for independent breeding by the parasitic individual.

Social environment and the benefits of parental care

Social interactions between families do not always result in parasitism. Sometimes both interacting sides can profit. For example, in cooperative breeders, some individuals postpone their personal reproduction in order to favour the reproduction of others, which was suggested to offer some of the strongest evidence of kin selection (Hamilton, 1964; Wilson, 1975). However, direct benefits such as communal territory defence, enhanced microclimate, enhanced foraging efficiency or nest/territory inheritance also favour the evolution of interactions between unrelated parents and between parents and offspring, including communal and cooperative breeding (e.g. Clutton-Brock, 2002; Bergmüller et al., 2007; Leadbeater et al., 2011).

Evidence of the direct benefits of communal breeding was found in a study on the parent bug Elasmucha grisea, a species where two females sometimes attend and defend their clutches jointly (Mappes et al., 1995). In a field experiment, Mappes et al. showed that communally guarding females had more eggs in their clutches than singly guarding females. The authors then confirmed this result in the laboratory by showing that joint unrelated females lost fewer eggs to ant predation than did single females, possibly because egg attendance is more than twice as effective with two females. The benefits of communal breeding are less clear in other species. In the burying beetle Nicrophorus defodiens, Eggert and Sakaluk (2000) showed that the presence of two females on a carcass did not reduce the risk of losing the carcass to other burying beetles. Scott (1994) suggested that communal breeding in the closely related Nicrophorus tomentosus reduces competition for carrion by fly maggots, a hypothesis that was later rejected by Eggert and Sakaluk (2000), who argued that large carrion flies cannot access carcasses once they are buried.

With regard to egg dumping (see earlier discussion; Tallamy, 2005), what appears to be a parasitic behaviour that is costly for the apparently parasitized individual might, in some cases, be beneficial for the dumper and the carer. Loeb et al. (2000) showed that females of the lace bug G. solani preferentially dump their eggs with kin, and that recipients gain indirect fitness by accepting these eggs. In their first bout of reproduction, significantly more of their own offspring survived to maturity in their first clutch than did controls without egg dumping (Loeb, 2003), most likely due to the predator dilution effect. In this case, egg dumping does not appear to be a parasitic strategy, but rather provides direct and indirect benefits of alternative reproductive tactics among closely related individuals.

The potential for intraspecific cooperation between females of the membracid Polyglypta dispar was suggested by Eberhard (1986). Multiple females were reported to oviposit in the same egg mass, and females sometimes adopted abandoned egg masses. Some guarding females attempted to prevent the visitor from ovipositing, whereas other guarding females just stepped aside. Guarding is a reproductively costly behaviour, since it delays the time to the next oviposition. Eberhard (1986) suggested that the probability of high genetic relatedness, due to philopatry contributes to the tendency for females to adopt abandoned egg masses. Furthermore, guarding females might benefit from the additional eggs, which are oviposited at the periphery of the egg mass, and Eberhard proposed that the eggs in the centre might become less subject to parasitism by parasitic wasps.

Parental care and family interactions need to be beneficial on balance for the offspring and the parent in order to evolve. Selection through direct or indirect benefits could have contributed to the evolution of parental care even if it is not purely directed to own genetic offspring, as described above by some exemplary studies. Such benefits could also partly explain why non-eusocial insect parents only rarely show sophisticated kin recognition and nepotism.

Ecological influences on social interactions

Ecological factors are expected to continue to shape selection on parental care once parental care originated. The evolutionary costs of certain amounts of parental care depend on the ecological context in which care is expressed. For instance, resource limitation in the environment is expected to modify the optimal investment in offspring, affecting the amount of resources transferred by parents to their offspring.

For example, in the European earwig (F. auricularia), females adjust the amount and duration of parental care to their own nutritional condition (Wong & Kölliker, 2012), which at least partly reflects food availability in the environment. Females provided food to fewer nymphs and for a shorter period of time, if their access to food was limited. Furthermore, in a study with the same earwig species, Meunier and Kölliker (2012b) showed that attendance by mothers can also be costly for offspring. Under food restriction, the usual fitness benefits of maternal presence for offspring (Kölliker, 2007) turn into a net reduction of offspring survival. The study could rule out the possibility that this effect was due to brood size adjustment by the female through filial cannibalism, as reported in the burying beetle N. vespilloides (Bartlett, 1987). Instead, it suggests direct competition for food between the female and her offspring under these conditions where the offspring pay the costs.

If offspring are not fully dependent on their parents (i.e. species with facultative care), they might take an active role in determining their own social environment. For example, work on the burrower bug S. cinctus showed that clutch joining initiated by the nymphs was especially high under insufficient food conditions (Agrawal et al., 2004). However, the consequences of joining between unrelated individuals (e.g. the increase in competition) were not investigated further. It would be interesting to test if females or nymphs exhibit discrimination against foreign offspring. The potential direct benefits of an increase in group size could explain why mothers accept foreign nymphs.

An increase in group size can also lead to local resource depletion and thus modify population dynamics. For example, Evans (1988) suggested that an increase in population density could result in an increase in intraspecific brood parasitism. This higher density can lead to scarcity of resources, such as breeding sites. For example, vertebrate carcasses of suitable quality are probably a scarce, unpredictable resource for burying beetles. Females of N. vespilloides fight for the ownership of carcasses and larger females usually manage to monopolize the carcass (Müller et al., 1990). However, the smaller female might stay near the carcass to lay her eggs for which the winning female will provide care. The lower the chances of finding another carcass on which no larger female is present, the more it pays a small female to stay and try to parasitize the winner's brood rather than leave. This results in costs for the larger female. Since larvae hatching from the parasite's eggs consume part of the available carrion mass, the number of offspring from the caring female was reduced.

Overall, these studies provide examples of how ecological conditions like population density or food availability influence variation in condition or parent–offspring relatedness. Other ecological factors, such as natural enemies, climatic change and the abiotic and biotic properties of the environment, can also influence selection through the social environment, for example by facilitating (or hindering) social interactions within and between families. This can affect social and family interactions and might modify or even reverse the usual benefits of parental care and turn them into costs paid by the parents and/or offspring.

Outlook

  1. Top of page
  2. Abstract
  3. Introduction
  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References

In this review, we have looked at former hypotheses regarding how ecological factors can affect benefits and costs of different forms of parental care, and how their effect on the evolution of parental care is expected to depend on the pre-existing life history of the species. When considering the likely complex relationships between ecology, life history and parental care in insects (see also Costa, 2006; Bonsall & Klug, 2011; Trumbo, 2012), we pointed out that the distinction between cause and effect is a critical one. Do some life-history traits facilitate the evolution of parental care or do the costs of parental care that evolve under particular ecological conditions lead to certain life histories? The wide variety of literature available, some of which has been presented here, is still short of systematic experimental studies that disentangle cause and effect between life history and ecology and that directly test factors that contribute to the evolution of parental care. The empirical evidence presented in Table 1 shows an over-representation of certain orders, e.g. the Blattodea. The large amount of work already available in these orders, together with the increasingly detailed molecular phylogeny of taxa, should lead to further investigations on the relationship among ecology, life history and phylogeny in the evolution of parental care.

To date, few studies have used comparative approaches to study the evolutionary history of parental care (Trumbo, 2012) but the following two are exemplary in demonstrating the scope that this approach has in answering evolutionary questions about the roles of ecology, life history, and the social environment in the evolution of parental care. Lin et al. (2004) used the molecular phylogeny of the treehopper subfamily Membracinae. Their results indicate that the ancestral state of the Membracinae is lack of maternal care and that there were three independent origins of egg attendance. The authors suggested that associated behaviours, life histories, and ecology may explain these origins, but the corresponding measurements were unfortunately not made. Gilbert and Manica (2010) went a step further and adopted a phylogenetic approach using quantitative data on body size, life history, and forms of care to test predictions about evolutionary associations between egg size, egg number (i.e. fecundity), and body size under different forms of parental care across 287 insect species from 16 orders. Their results showed that evolutionary changes in parental care were associated with lifetime fecundity rather than with egg size and that egg size was only influenced by body size (Gilbert & Manica, 2010). Such phylogenetic studies hold great promise to further our understanding of the evolutionary origin of parental care when they are combined with close investigations and comparisons of the ecology, life history, and the social environment (Trumbo, 2012). This would comprise a large enough number of species, which show diversity in the forms of care within and among lineages as well as reliable measures of ecological factors and life history.

Besides phylogenetic work, more empirical studies investigating the evolution of parental care are required, and insects are probably uniquely suitable study systems to this end. Compared with mammals and birds that exhibit obligate forms of care, insects display a wide variability regarding the presence or absence of different forms of care, and regarding the degree of offspring dependence on these forms of care. Nevertheless, detailed experimental research on parental care and social interactions within and between families has been limited to comparably few species. Besides the investigation of causes and consequences of parental care and social environments, there is still also a need for basic natural history work because our knowledge of the diversity in the forms and extent of care is still limited in many taxa (Trumbo, 2012). Finally, the typically shorter generation time of insects compared with other model systems, and their easier maintenance under laboratory conditions enable us to investigate life-history traits associated with divergent patterns of care between closely related species, as well as the effect of specific environmental factors (e.g. variation in predation pressure or food resources) on long-term changes in the form and strength of parental care. Thus, insects are a highly interesting and suitable system to address open key questions on the evolution of parental care.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References

Many thanks to Patrick Alexander, Erhard Strohm, Gudrun Herzner, Per Smiseth, Kiyoto Maekawa, and Jennifer Hamel for kindly providing us with the pictures displayed in Fig. 1. Furthermore, we are grateful to Per T. Smiseth, Klaus Reinhardt and three anonymous referees for providing very useful comments on earlier drafts of the manuscript. Our research is supported by the Swiss National Science Foundation (grant-no. PP00A-119190 to MK).

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  4. Ecology, life history and insect parental care
  5. Social environment and the evolution of insect parental care
  6. Outlook
  7. Acknowledgements
  8. References
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