Subsociality in halictine bees

To look for the occurrence and the significance of brood care in social evolution, I reared six eusocial halictine bee species in laboratory cages enabling the observation of intranest behaviour: Lasioglossum (Evylaeus) laticeps, L. (E.) pauxillum, L. (E.) nigripes, L. (E.) euboeensis, Halictus (Halictus) scabiosae and L. (E.) fulvicorne. All of them were subsocial, each mother caring for her brood. Brood cells were sealed after oviposition with earthen plugs; they were then reopened, visited and closed again. These observations plus the reports in the literature on eleven eusocial species indicate that seventeen species of eusocial halictine bees provide parental care, i.e. are subsocial. Brood care, subsociality, is strongly associated with eusociality. To study reversal from eusociality to subsociality, I have reared the non-eusocial form of two species within which there are or have been eusocial forms: Halictus (H.) rubicundus and Lasioglossum (E.) fratellum. They are secondarily solitary, having lost worker brood. However, both species still show brood care. This suggests that in transitions to eusociality, brood care antedated eusociality. To further examine this issue I reared two truly solitary species that are not derived from eusocial ancestors: Lasioglossum (E.) villosulum and L. (L.) quadrinotatum. Unlike secondarily solitary species, females of both these species close their brood cells after oviposition and ignore their progeny thereafter. This association strongly suggests that the subsocial route with maternal brood care is the route to eusociality in halictine bees.     

A review of the ecological parameters and implications of subsociality in Parastrachia japonensis (Hemiptera: Cydnidae), a semelparous species that specializes on a poor resource

Subsocial behavior or postovipositional parental care in insects has evolved in response to a variety of environmental stresses and ranges from briefly guarding eggs after oviposition to elaborate nidification and provisioning behaviors. Investment in parental care bears various costs, and should not continue beyond the point at which the costs to future reproductive success exceed the benefits to current reproductive effort. Progressive provisioning is a rare form of subsociality in insects. Females of the subsocial shield bug Parastrachia japonensis progressively provision their nymph-containing nests with drupes of the single resource, Schoepfia jasminodora, and this provisioning drastically enhances offspring survival. A female rears only one brood throughout her lifetime and continues provisioning the brood until about the third larval stadium, when the female dies. Thus, the female's entire reproductive effort is expressed in the success of that one brood, which suggests a reproductive strategy with enormous costs and risks. Why has such an extreme life history evolved in this species? Here, to answer that question and to contribute to our understanding of the evolutionary implications of subsocial behavior, in particular, progressive provisioning, we review what we have discovered about the ecological parameters of subsociality in this species during a long-term field study. We also discuss these parameters in P. japonensis in reference to other subsocial insects and related species and conclude with a suggestion that semelparity and progressive provisioning in this species are extreme adaptations to evolving complete dependency on an unreliable resource.     

One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig

Whether to reproduce once or multiple times (semelparity vs. iteroparity) is a major life-history decision that organisms have to take. Mode of parity is usually considered a species characteristic. However, recent models suggested that population properties or condition-dependent fitness payoffs could help to maintain both life-history tactics within populations. In arthropods, semelparity was also hypothesised to be a critical pre-adaptation for the evolution of maternal care, semelparous females being predicted to provide more care due to the absence of costs on future reproduction. The aim of this study was to characterize potential fitness payoffs and levels of maternal care in semel- and itero-parous females of the European earwig Forficula auricularia. Based on 15 traits measured in 494 females and their nymphs, our results revealed that iteroparous females laid their first clutch earlier, had more eggs in their first clutch, gained more weight during the 2 weeks following hatching of the first clutch, but produced eggs that developed more slowly than semelparous females. Among iteroparous females, the sizes of first and second clutches were significantly and positively correlated, indicating no investment trade-off between reproductive events. Iteroparous females also provided more food than semelparous ones, a result contrasting with predictions that iteroparity is incompatible with the evolution of maternal care. Finally, a controlled breeding experiment reported full mating compatibility among offspring from females of the two modes of parity, confirming that both types of females belong to one single species. Overall, these results indicate that alternative modes of parity represent coexisting life-history tactics that are likely to be condition-dependent and associated with offspring development and specific levels of maternal care in earwigs.     

Provisioning control during maternal care by the earwig Anisolabis maritima (Dermaptera: Anisolabididae): Do mothers adjust provisioning according to offspring need?

Provisioning offspring is an important form of parental care for the improvement of offspring survival and growth. Because provisioning can be costly for parents, parents may change their investment levels in response to offspring need and begging signals. Anisolabis maritima is a cosmopolitan species of earwig that shows subsocial behavior. Females progressively provision their young in soil burrows. The present study investigated whether A. maritima mothers carry food to the nest for their offspring (nymphs) and whether the mothers adjust the amount of food carried to the burrow according to the degree of the nymphs’ hunger. Through laboratory experiments, I found that mothers carried food to sites where more nymphs were present, and more food to broods of more hungry nymphs. These results have revealed that mothers recognize the presence of offspring and the degree of their hunger. This study, therefore, indicates the presence of offspring begging signals in A. maritima.     

Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonid fishes

The selective pressures involved in the evolution of semelparity and its associated life-history traits are largely unknown. We used species-level analyses, independent contrasts, and reconstruction of ancestral states to study the evolution of body length, fecundity, egg weight, gonadosomatic index, and parity (semelparity vs. degree of iteroparity) in females of 12 species of salmonid fishes. According to both species-level analysis and independent contrasts analysis, body length was positively correlated with fecundity, egg weight, and gonadosomatic index, and semelparous species exhibited a significantly steeper slope for the regression of egg weight on body length than did iteroparous species. Percent repeat breeding (degree of iteroparity) was negatively correlated with gonadosomatic index using independent contrasts analysis. Semelparous species had significantly larger eggs by species-level analysis, and the egg weight contrast for the branch on which semelparity was inferred to have originated was significantly larger than the other egg weight contrasts, corresponding to a remarkable increase in egg weight. Reconstruction of ancestral states showed that egg weight and body length apparently increased with the origin of semelparity, but fecundity and gonadosomatic index remained more or less constant or decreased. Thus, the strong evolutionary linkages between body size, fecundity, and gonadosomatic index were broken during the transition from iteroparity to semelparity. These findings suggest that long-distance migrations, which increase adult mortality between breeding episodes, may have been necessary for the origin of semelparity in Pacific salmon, but that increased egg weight, leading to increased juvenile survivorship, was crucial in driving the transition. Our analyses support the life-history hypotheses that a lower degree of repeat breeding is linked to higher reproductive investment per breeding episode, and that semelparity evolves under a combination of relatively high juvenile survivorship and relatively low adult survivorship.     

Interaction between parental care and sibling competition: parents enhance offspring growth and exacerbate sibling competition

Species with elaborate parental care often also show intense sibling competition over resources provided by parents, suggesting joint evolution of these two traits. Despite this, the evolution of elaborate parental care and the evolution of intense sibling competition are often studied separately. Here, we examine the interaction between parental food provisioning and sibling competition for resources through the joint manipulation of the presence or absence of parents and brood size in a species with facultative parental care: the burying beetle Nicrophorus vespilloides. The effect of the interaction between the presence or absence of parents and brood size was strong; brood size had a strong effect on growth when parents provided care, but no effect when parents were absent. As in previous studies, offspring grew faster when parents were present than when parents were absent, and offspring grew faster in smaller broods than in larger broods. Our behavioral observations showed that brood size had a negative effect on both the amount of time parents spent providing resources to individual offspring and the offspring's effectiveness of begging, confirming that the level of sibling competition increased with brood size. Furthermore, offspring in larger broods shifted more from begging toward self-feeding as they grew older compared to offspring in small broods. Our study provides novel insights into the joint evolution of parental care and sibling competition, and the evolution of offspring begging signals. We discuss the implications of our results in light of recent theoretical work on the evolution of parental care, sibling competition, and offspring begging signals.     

Allocation of Male Parental Care in Relation to Paternity Within and Among Broods of the Common Yellowthroat (Geothlypis trichas)

The relationship between male parental care and paternity has been investigated in a number of avian species, but in many cases the influences of confounding factors, such as variation in male and territory quality, were not addressed. These sources of variation can be controlled for by making within-male comparisons between successive broods or within-brood comparisons between groups of fledglings in a divided brood. We studied the relationship between male parental care and paternity in the common yellowthroat ( Geothlypis trichas ) at three levels: between groups of fledglings in divided broods, between first and second broods of the same pair, and among all broods in the population. In this study we proposed three hypotheses: first, males in double-brooded pairs should provide relatively more parental care to broods in which they have higher paternity; secondly, after fledging and brood division, males should provide more care to related offspring; and finally, among all broods in the population, paternity should be related positively to male parental care. Brood division occurred in many of the broods studied; however, broods were not divided according to fledgling size or paternity. Furthermore, within divided broods, males fed within-pair and extra-pair fledglings at similar rates. For sequential broods of the same pair, male feeding rates were not associated with differences in paternity between broods. Among all broods in the population, males did not provide relatively less care to broods containing unrelated young. The lack of a relationship between male parental care and paternity suggests that either males cannot assess their paternity or the costs of reducing male parental care outweigh the benefits.     

Stochasticity and spatial coexistence of semelparity and iteroparity as life histories

We investigate conditions enabling long-term coexistence of semelparity (reproducing only once per lifetime) and iteroparity (repeated spells of reproduction in subsequent breeding seasons). Bulmer (1985, 1994) has transferred the study of the fitness merit of reproducing semelparously vs. iteroparously into a density-dependent system, using an invasion scenario with an abundant resident population of one reproductive strategy and a rare mutant invader population of another reproductive strategy. For stable population dynamics, Bulmer (1994) derived condition v + P _A < 1 (P _A is adult survival and v is the ratio of offspring number of the iteroparous type over that of the semelparous type) where a semelparous population cannot be invaded by an iteroparous strategy. In order to study the generalisation of Bulmer's results in spatial population dynamics, we generate a population system consisting of a linear string of habitable sub-units. The sub-units are semi-independent, obeying discrete-time Ricker dynamics in renewal, but they are close enough for dispersing individuals to couple them together. At each time step, a random fraction of individuals in each sub-unit disperses into neighbourhood. In this setting, we observe long-term persistence of semelparity and iteroparity when dispersal is stochastic and positively autocorrelated. Stochasticity in dispersal creates fluctuating local dynamics and thus permits long-term persisting coexistence of semelparity and iteroparity even in the parameter region where Ricker dynamics are stable and the Bulmer inequality is true. Positively autocorrelated, in contrast to negatively autocorrelated dispersal time-series, promoted coexistence between semelparity and iteroparity.     

COEVOLUTIONARY FEEDBACKS BETWEEN FAMILY INTERACTIONS AND LIFE HISTORY

Families with parental care show a parent–offspring conflict over the amount of parental investment. To date, the resolution of this conflict was modeled as being driven by either purely within‐brood or between‐brood competition. In reality the partitioning of parental resources within‐ versus between‐broods is an evolving life history trait, which can be affected by parent–offspring interactions. This coevolutionary feedback between life history and family interactions may influence the evolutionary process and outcome of parent–offspring coadaptation. We used a genetic framework for a simulation model where we allowed parental parity to coevolve with traits that determine parental investment. The model included unlinked loci for clutch size, parental sensitivity, baseline provisioning, and offspring begging. The simulation showed that tight coadaptation of parent and offspring traits only occurred in iteroparous outcomes whereas semelparous outcomes were characterized by weak coadaptation. When genetic variation in clutch size was unrestricted in the ancestral population, semelparity and maximal begging with poor coadaptation evolved throughout. Conversely, when genetic variation was limited to iteroparous conditions, and/or when parental sensitivity was treated as an evolutionarily fixed sensory bias, coadapted outcomes were more likely. Our findings show the influence of a feedback between parity, coadaptation, and conflict on the evolution of parent–offspring interactions.     

Adaptive secondary sex ratio adjustments via sex-specific infanticide in a bird

Infanticide is easiest to understand when it involves killing the offspring of others [1], but a parent may also kill its own offspring if the sacrifice of currently dependent young leads to higher survival of brood mates [2] or an improvement in the parent's likely future reproduction [3]. However, sex-specific infanticide by parents of their own offspring, although occurring in some human societies [4], is rare across species. Its rarity may be because killing one sex combines wasted parental effort with consequent biases in population sex ratios that are detrimental for the fitness of the overproduced sex [5-7]. We show that killing male offspring can be advantageous to Eclectus parrot (Eclectus roratus) mothers even though frequency-dependent selection then elevates the reproductive value of sons above that of daughters. In poorer-quality nest hollows, broods with a single female nestling had higher reproductive value than broods in which the female had a younger brother. Our data demonstrate frequent targeted removal of male nestlings within 3 days of hatching in these specific brood types and nesting conditions. The ability of Eclectus parrots to perceive the sex of their offspring relatively early may favor decisions to kill one sex before further investment in parental care.     

Asynchronous hatching provides females with a means for increasing male care but incurs a cost by reducing offspring fitness

In species with biparental care, sexual conflict occurs because the benefit of care depends on the total amount of care provided by the two parents while the cost of care depends on each parent's own contribution. Asynchronous hatching may play a role in mediating the resolution of this conflict over parental care. The sexual conflict hypothesis for the evolution of asynchronous hatching suggests that females adjust hatching patterns in order to increase male parental effort relative to female effort. We tested this hypothesis in the burying beetle Nicrophorus vespilloides by setting up experimental broods with three different hatching patterns: synchronous, asynchronous and highly asynchronous broods. As predicted, we found that males provided care for longer in asynchronous broods whereas the opposite was true of females. However, we did not find any benefit to females of reducing their duration of care in terms of increased lifespan or reduced mass loss during breeding. We found substantial negative effects of hatching asynchrony on offspring fitness as larval mass was lower and fewer larvae survived to dispersal in highly asynchronous broods compared to synchronous or asynchronous broods. Our results suggest that, even though females can increase male parental effort by hatching their broods more asynchronously, females pay a substantial cost from doing so in terms of reducing offspring growth and survival. Thus, females should be under selection to produce a hatching pattern that provides the best possible trade‐off between the benefits of increased male parental effort and the costs due to reduced offspring fitness.     

Maternal provisioning and possible joint breeding in the burrower bug Adomerus triguttulus (Heteroptera: Cydnidae)

Subsocial burrower bugs (Heteroptera: Cydnidae) provide unique opportunities to investigate evolutionary ecological questions regarding parental provisioning and family dynamics. Observations and marked nutlet‐setting experiments in the field showed that Adomerus triguttulus females progressively delivered mint nutlets into nests harbouring nymphs under the litter. More than one female often attended nymphs, but not eggs, in a nest in the field. The number of nymphs aggregating in a nest with a single female was usually smaller than that in a nest with two females, suggesting the joining of different families and facultative joint parental care. There was a positive correlation between the number of nutlets delivered and the number of nymphs in a nest. The number of attendant females also affected the amount of provisioning; more nutlets were found for second‐instar broods with more females. The effect of brood size on provisioning was confirmed for families under laboratory rearing. Maternal provisioning also varied with the developmental stage of offspring; second‐instar broods received more nutlets than first‐instar broods, with a temporal decrease in provisioning during the moulting of nymphs. Considering the growing evidence of food solicitation signals of young in subsocial insects, the observed finely tuned supply of food by the female could be induced by begging signals from the nymphs.     

Temporal Variation in Decisions about Parental Care in Bluegill, Lepomis macrochirus

Parental investment theory states that an individual will trade‐off present and future reproductive potential to maximize lifetime reproductive success. Only when parental care is costly in terms of reduced future reproductive potential should individuals be sensitive to changes in the value of current offspring and adjust their care. Here, we examine temporal variation in parental care decision‐making in bluegill (Lepomis macrochirus), in which care is provided by males called ‘parentals’. Previous research has shown that parentals that nest early in the breeding season are in higher energetic condition than those that nest later, and early nesting males appear not to pay an opportunity cost to their care in terms of reduced future reproductive potential. Early nesting males also may have higher paternity in their broods than later nesting males. To examine the parental care decisions made by early and mid‐season nesting parentals, we experimentally reduced males’ perceived paternity by swapping eggs between nests. We found that experimental males that nested early in the breeding season adjusted their brood defence behaviour similarly to control males, which had sham egg swaps performed. Conversely, experimental males that nested mid‐season significantly decreased their brood defence behaviour after the manipulation as compared with control males. Thus, unlike mid‐season nesting males, early nesting males appear relatively insensitive to changes in brood value (paternity), possibly because early nesting males pay little cost in terms of reduced future reproductive potential to providing full care or because these males have a predisposition to high paternity.     

Irreversible transfer of brood care duties and insights into the burden of caregiving in incipient subterranean termite colonies

1. In incipient termite colonies, biparental brood care rapidly shifts towards alloparental brood care. This transition was suggested to recapitulate the evolutionary trajectory from subsocial wood roach ancestors to eusociality in termites. 2. Incipient colonies of the subterranean termite Coptotermes gestroi (Wasmann) were investigated to determine if this transition was irreversible and if the burden of brood care on the first alloparents could be measured. To do so, the initial size of the work force necessary for an incipient colony to survive once the brood care became alloparental was determined. 3. The results of the study show that within 5 months after foundation, brood care duties were fully transferred to workers and the primary reproductives became irreversibly dependent on these workers for survival, reproduction, and colony growth. 4. Once the brood care became strictly alloparental, the presence of a single worker was enough to maintain the survival of the king and queen, confirming that ‘reversed parental care’ was also achieved. However, major brood loss and suppressed egg‐laying activity from the queen was observed, suggesting that the burden of brood care was too high for a single worker to absorb. Therefore, once brood care has shifted to alloparents, a critical number of workers is necessary to prevent brood loss and initiate colony growth. 5. As the initial cost of brood care is rapidly absorbed with colony growth in termites, the performance in brood care of the first few alloparents in a subsocial wood roach ancestor may have contributed to the emergence of eusociality in this clade.     

Effect of predators and host phenology on the maternal and reproductive behaviors ofGargaphia lace bugs (Hemiptera: Tingidae)

Lace bugs of the genus Gargaphia specialize on taxonomically and ecologically diverse host plants. To examine the impact of predation pressure and host phenology on Gargaphia subsocial and reproductive behavior, we compared G. tiliae, a woodland species restricted to riparian trees in the genus Tilia, and G. solani, a specialist on Solanum in early successional habitats. Both lace bug species exhibit maternal care of eggs and nymphs. Predator densities associated with Solanum were higher than those associated with Tilia and were correlated with higher levels of maternal aggression exhibited by G. solani. In both habitats, artificial exclusion of predators significantly increased nymphal survivorship over maternally guarded broods. Both species reduced the costs associated with maternal care by ovipositing into the egg masses of conspecifics. Gargaphia solani and G. tiliae differed most strikingly in voltinism and thus the potential for iteroparity. Leaf age determined the reproductive future of G. tiliae nymphs independent of photoperiod or temperature. Feeding on plants with young foliage was sufficient to trigger oviposition. Constraints imposed by host plants on life-history patterns and maternal options are discussed.     

Brood desertion in Kentish plover: the value of parental care

To understand the evolution of parental care, one needs to estimatethe payoffs from providing care for the offspring and from terminatingcare and deserting them. In this study we estimated the payofffrom care provision, and in a companion paper we analyze thepayoff from offspring desertion. In the current study we experimentallyinvestigated the influence of the number and sex of attendingparents on growth and survival of offspring in the Kentish ploverCharadrius alexandrinus, in two sites (A and B). Either the maleor the female parent was removed from some broods at hatchingof the chicks (female-only and male-only broods, respectively),whereas in control broods both parents were allowed to attendtheir young. At site A survival of the chicks was lower in uniparental(male-only and female-only) broods than in control broods, whereaswe found no difference in brood survival at site B. Brood survivaldecreased over the season. Removal of either parent did not influencethe growth of the young, although growth varied over the breeding season,and it was significantly different between the sites. Theseresults suggest that the payoff from parental care decreasesover the breeding season and that the value of parental care(i.e., the contribution of parents to the survival of theiryoung) may depend on the environment.     

Male "mixed" reproductive strategies in biparental species: Trivers was probably right, but why?

Trivers proposed that, if parental care by both sexes is advantageous, males should practice a "mixed" strategy of seeking extrapair copulations, while restricting their parental investment to offspring of social mates. We explore circumstances under which males should limit their parental care in the predicted manner. We find that Trivers's "mixed" strategy will generally be evolutionarily stable so long as either socially monogamous or polygynous males usually sire more offspring per brood from a social mate than they typically sire in broods of extrapair mates. Polygynous males should spread investment across their home nests unless the expected number of chicks sired in them differs widely. Whether polygynous males should restrict paternal care to social mates' offspring hinges additionally on resident male investment in broods containing extrapair young: if resident males contribute minimally, some investment by a polygynous extrapair male becomes more advantageous. Recently reviewed data on extrapair fertilization distributions within monogamous and polygynous passerines suggest that extrapair offspring often predominate numerically within their broods, consistent with sperm expenditure theory. Nevertheless, most species conform to the model's criterion regarding relative parentage levels in broods of social versus extrapair mates. Patterns of extrapair parentage thus appear sufficient to stabilize biparental care systems.     

Alloparental care in the sea: Brood parasitism and adoption within and between two species of coral reef Altrichthys damselfish?

The evolution of parental care opens the door for the evolution of brood parasitic strategies that allow individuals to gain the benefits of parental care without paying the costs. Here we provide the first documentation for alloparental care in coral reef fish and we discuss why these patterns may reflect conspecific and interspecific brood parasitism. Species‐specific barcodes revealed the existence of low levels (3.5% of all offspring) of mixed interspecific broods, mostly juvenile Amblyglyphidodon batunai and Pomacentrus smithi damselfish in Altrichthys broods. A separate analysis of conspecific parentage based on microsatellite markers revealed that mixed parentage broods are common in both species, and the genetic patterns are consistent with two different modes of conspecific brood parasitism, although further studies are required to determine the specific mechanisms responsible for these mixed parentage broods. While many broods had offspring from multiple parasites, in many cases a given brood contained only a single foreign offspring, perhaps a consequence of the movement of lone juveniles between nests. In other cases, broods contained large numbers of putative parasitic offspring from the same parents and we propose that these are more likely to be cases where parasitic adults laid a large number of eggs in the host nest than the result of movements of large numbers of offspring from a single brood after hatching. The evidence that these genetic patterns reflect adaptive brood parasitism, as well as possible costs and benefits of parasitism to hosts and parasites, are discussed.     

Effects of parental care on offspring growth in the Korean wood-feeding cockroach, <Emphasis Type="Italic">Cryptocercus kyebangensis</Emphasis>

The objective of this study was to measure the possible effects of prolonged parental care on offspring growth in Korean wood-feeding cockroaches, Cryptocercus kyebangensis. In the field-caught subsocial woodroaches of C. kyebangensis, offspring with both parents were greater in both head width and body weight than those with single parents. Manipulation experiments showed that offspring separated from their parents could survive independently without parents, but they grew more rapidly when they remained with their parents. In particular, the effects of parental care on offspring growth were found to be stronger in groups with both parents than those with single parents. These results suggest that the prolonged parental care evolved in Cryptocercus has a significant impact on offspring growth. Electronic Publication     

Macroecology of parental care in arthropods: higher mortality risk leads to higher benefits of offspring protection in tropical climates

The intensity of biotic interactions varies around the world, in such a way that mortality risk imposed by natural enemies is usually higher in the tropics. A major role of offspring attendance is protection against natural enemies, so the benefits of this behaviour should be higher in tropical regions. We tested this macroecological prediction with a meta‐regression of field experiments in which the mortality of guarded and unguarded broods was compared in arthropods. Mortality of unguarded broods was higher, and parental care was more beneficial, in warmer, less seasonal environments. Moreover, in these same environments, additional lines of defence further reduced offspring mortality, implying that offspring attendance alone is not enough to deter natural enemies in tropical regions. These results help to explain the high frequency of parental care among tropical species and how biotic interactions influence the occurrence of parental care over large geographic scales. Finally, our findings reveal that additional lines of defences – an oftentimes neglected component of parental care – have an important effect on the covariation between the benefits of parental care and the climate‐mediated mortality risk imposed by natural enemies.