Infanticide and control of reproduction in cooperative and communal breeders

Many communal breeders are characterized by a conflict over who gets to reproduce, with dominant individuals often claiming the largest share of reproduction in the group. How do dominants control breeding in these species? Although infanticide has often been invoked as a means of control, previous theoretical work on indiscriminate killing of young did not support this idea. There is, however, increasing evidence from field studies in both vertebrates and insects that infanticidal individuals can discriminate between their own offspring and those of other group members, and thus avoid the risk of accidentally killing their own progeny. In a simple game-theoretical model we demonstrate that the capacity for discriminate infanticide can promote high reproductive skew even though few or no offspring are actually killed. When discrimination is good and offspring are cheap to produce, the threat of infanticide prevents the subordinate cobreeder from adding many young to the joint brood, and no killing need occur. High levels of infanticide tend to occur only when discrimination is poor, costs of offspring production are low and/or relatedness is low.     

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.     

Group composition affects male reproductive partitioning in a cooperatively breeding cichlid

Individuals within groups of cooperatively breeding species may partition reproduction, with the dominant pair often taking the largest share. The dominant's ability to reproductively control subordinates may depend on differences in competitive ability, due to, e.g. body size differences, but may also depend on the number of same‐sex competitors inside the group. We tested experimentally whether subordinates reproduce more when these subordinates are large or when a second subordinate of the same sex need to be controlled by the dominants, using the cooperatively breeding cichlid Neolamprologus pulcher. Dominant pairs were assisted by a large and a small unrelated subordinate; sexes of these fish were varied in a full‐factorial design (giving four treatments). Dominant males lost significantly more parentage to the large subordinate male when a small subordinate male was also present, compared to when a small subordinate female was present. However, subordinate paternity was generally low and did not significantly curb total dominant male reproductive output, which was more affected by the sizes and numbers of reproductive females present inside his group. Dominant female maternity, clutch sizes and total output did not depend on the treatments. Subordinate–subordinate reproduction was virtually absent (one out of 874 offspring). Female subordinates were more likely to provide care for their own broods. In contrast, male subordinates did not adjust their level of care to their parentage. Variability in female subordinate alloparental brood care was particularly high, with females showing more care than males in general. We also detected effects of growth rate and food ration on parentage independent of the treatments, most notably: (i) a trade‐off between dominant male growth rate and paternity; (ii) a decrease in dominant male paternity with increasing food ration; (iii) a positive effect of growth rate on paternity in small males. We conclude that dominant males should be sensitive to the number and sizes of subordinate males present in their group, particularly when these subordinates are not helpful or grow fast, and food is plentiful. Dominant females should be less sensitive, because female subordinates do not appear to impose reproductive costs and can be helpful through alloparental brood care.     

Parental care, cost of reproduction and reproductive skew: a general costly young model

Understanding the mechanisms by which animals resolve conflicts of interest is the key to understanding the basis of cooperation in social species. Conflict over reproductive portioning is the critical type of conflict among cooperative breeders. The costly young model represents an important, but underappreciated, idea about how an individual's intrinsic condition and cost of reproduction should affect the resolution of conflict over the distribution of reproduction within a cooperatively breeding group. However, dominant control in various forms and fixed parental care (offspring fitness dependent solely on total brood size) are assumed in previous versions of costly young models. Here, we develop a general costly young model by relaxing the restrictive assumptions of existing models. Our results show that (1) when the complete-control assumption is relaxed, the costly young model behaves very differently from the original model, and (2) when the fixed parental care assumption is relaxed, the costly young-costly care model displays similar predictions to the tug-of-war model, although the underlying mechanisms causing these similar patterns are different. These results, we believe, help simplify the seemingly divergent predictions of different reproductive skew models and highlight the importance of studying the group members' intrinsic conditions, costs of producing young, and costs of parental care for understanding breeding conflict resolution in cooperatively breeding animals.     

PROXIMATE AND ULTIMATE CONTROLS ON LIFE-HISTORY VARIATION: THE EVOLUTION OF LITTER SIZE IN WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS)

Recruitment of litter-mates of nest-box-inhabiting white-footed mice was monitored to study the evolution of litter size. The frequency distribution of litter sizes was nonsymmetrical, and the most frequent litter size was less than the optimum. This was not the result of differential parental survival, which was independent of litter size produced. Recruitment remained constant or increased slightly to a peak in litters of five young, and then dropped precipitously for larger litters. The single optimum litter size of five did not appear to have any physiological correlates. Instead, the equally low probability of successful recruitment of any young from any given litter may have given rise to a bet-hedging strategy of frequent iterated reproductions. A theoretical analysis of optimal parental investment in offspring was initiated under the assumption that optimal brood size represents a maximization of differences between age-specific costs and benefits of reproduction, both of which should be measured in constant currency of inclusive fitness. In the past, benefit has been measured by current fecundity, and cost by residual reproductive value. However, reproductive value is an appropriate estimate of inclusive fitness only for organisms in which parental investment has little effect on the subsequent survival of offspring to reproductive age. Reproductive value weighted by offspring survival and devalued by the degree of genetic relatedness defines a new currency, replacement value, which is more appropriate for evaluating the costs and benefits of parent-offspring conflict over parental investment in current as opposed to future young. Total parent-offspring conflict intensifies with increases in current brood size. For species with severe reproductive constraints, such as post-partum estrus in white-footed mice, such conflict may force parents to curtail investment in current offspring at or near parturition of subsequent litters, even if that means reducing the survival of current young.     

The number of subordinates moderates intrasexual competition among males in cooperatively breeding meerkats

For dominant individuals in cooperatively breeding species, the presence of subordinates is associated with both benefits (i.e. increased reproductive output and other group-living benefits) and costs (i.e. intrasexual competition on reproduction). The biological market theory predicts that dominant individuals are tolerant to same-sex group members when there are only a few subordinates, so as to maximize their own reproductive success. We investigated factors affecting aggression by dominant males and submission by subordinate males for a cooperatively breeding mammal, meerkats, Suricata suricatta. In this species, reproductive conflict occurs between the dominant male and the non-offspring males. As predicted, the number of subordinates in a group was positively associated with the aggression frequency by the dominant male and with the submission frequency by the subordinate males. Relative to the aggression frequency against male offspring, the frequency of aggression against non-offspring males was comparable in small groups, but was higher in large groups. These results indicate that reproductive conflict is present between the dominant male and the non-offspring males but is moderated in groups with small numbers of subordinates. This study provides an empirical data agreeing with the biological market theory in the context of intrasexual competition in cooperatively breeding species.     

Genetic monogamy in single-male groups of acorn woodpeckers, Melanerpes formicivorus

Acorn woodpeckers have one of the most complex social systems of any bird species. Breeding units range in size from monogamous pairs to groups of 15 birds that include multiple breeding males and females as well as nonreproductive helpers-at-the-nest. Groups form when young remain at their natal nest to help their parents breed or when single-sex coalitions of siblings disperse to fill a reproductive vacancy on another territory. Plural breeding and helping behaviour are thought to be favoured through indirect fitness benefits for individuals that would otherwise be unable to breed due to a shortage of reproductive vacancies on territories with acorn stores. We report the results of multi-locus DNA fingerprinting of 51 offspring from 18 nests of 16 socially monogamous pairs of acorn woodpeckers. If socially monogamous females mate outside the pair-bond, indirect fitness benefits for cobreeders and helpers will be significantly reduced. Monogamous pairs accounted for all but one of the 51 offspring we tested; the single exception was apparently sired by the putative father, but the putative mother was excluded from maternity. Our results indicate that individuals remaining on their natal territories as helpers are generally the genetic offspring of the pair they help. They also suggest that single-sex coalitions offspring dispersing together from nests of socially monogamous pairs will be full-siblings.     

Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal

In cooperatively breeding species, subordinates typically suffer strong constraints on within-group reproduction. While numerous studies have highlighted the additional fitness benefits that subordinates might accrue through helping, few have considered the possibility that subordinates may also seek extra-group matings to improve their chances of actually breeding. Here, we show that subordinate males in cooperative meerkat, Suricata suricatta, societies conduct frequent extraterritorial forays, during periods of peak female fertility, which give rise to matings with females in other groups. Genetic analyses reveal that extra-group paternity (EGP) accrued while prospecting contributes substantially to the reproductive success of subordinates: yielding the majority of their offspring (approx. 70%); significantly reducing their age at first reproduction and allowing them to breed without dispersing. We estimate that prospecting subordinates sire 20-25% of all young in the population. While recent studies on cooperative birds indicate that dominant males accrue the majority of EGP, our findings reveal that EGP can also arise from alternative reproductive tactics employed exclusively by subordinates. It is important, therefore, that future attempts to estimate the fitness of subordinate males in animal societies quantify the distribution of extra-group as well as within-group paternity, because a substantial proportion of the reproductive success of subordinates may otherwise go undetected.     

Cooperation, conflict, and crèching behavior in goldeneye ducks

Crèching behavior, or brood amalgamation, results in offspring being reared by adults other than their genetic parents. Although a variety of hypotheses have been proposed to explain this behavior, most assume either that brood amalgamation is accidental (i.e., nonselected) or that adoption of young is selected for because of social benefits to the young and/or adopting parents. We propose, instead, that brood amalgamation is a function of two separate processes: brood desertion and brood adoption. To examine brood desertion, we develop a graphic model to predict when parents should abandon their young and we test this model experimentally for the Barrow's goldeneye (Bucephala islandica). As predicted, females deserted their offspring when the size of the brood was experimentally reduced. Brood adoption occurred when deserted ducklings joined other broods. However, the success of ducklings in doing so was strongly dependent on the availability of potential host broods and on the age of the recipient broods. Foreign ducklings were readily accepted into young broods (<10 d old) but invariably were rejected from old broods. We could detect no benefits or costs of brood adoption to the host females, contrary to the expectations of a social benefit hypothesis. Our experiments indicate that Crèching behavior is driven by selection on adults to abandon their brood when the benefits of continued investment are outweighed by the reduction in future reproduction and selection on deserted ducklings to join other broods to obtain parental care. Rather than a form of cooperative brood care, Crèching in goldeneyes is perhaps best considered as a form of reproductive parasitism, entailing parent-offspring conflict over brood desertion and intergenerational conflict over adoption of abandoned young.     

Costly Solicitation, Timing of Offspring Conflict, and Resource Allocation in Plants

The theory of parent–offspring conflict is extended toplants that produce many offspring in one reproductive event.The energetic cost of begging signals and the timing of offspringconflict are explicitly taken into account. We find that ifthe indirect costs of increased provisioning of selfish offspringare borne by their brood mates, then offspring are selectedto solicit in so costly a way that a substantial part of parentalinvestment in a brood goes to solicitation rather than offspring'sgrowth and survival. Consequently, offspring conflict oftenresults in smaller seed size than the parental optimum in theabsence of conflict, although each offspring still consumesmore resources than the amount its mother is willing to give.While the optimal sex allocation can be shown to be independentof solicitation and sibling conflict, the overall reproductiveeffort is always lowered by parent–offspring conflict.The timing of offspring conflict during the period of parentalinvestment is demonstrated to be an important factor that influencesthe outcome of parent–offspring conflict. The more resourcesare allocated to individual offspring before the occurrenceof offspring solicitation, the less offspring should solicit,and hence the closer the offspring size to the parental optimum.Copyright 2000 Annals of Botany Company Evolutionarily stable strategy, parent–offspring conflict, parental investment, reproductive resource allocation, seed size, solicitation, timing of offspring conflict     

Females compensate for moult‐associated male nest desertion in Hooded Warblers

Uniparental offspring desertion occurs in a wide variety of avian taxa and usually reflects sexual conflict over parental care. In many species, desertion yields immediate reproductive benefits for deserters if they can re‐mate and breed again during the same nesting season; in such cases desertion may be selectively advantageous even if it significantly reduces the fitness of the current brood. However, in many other species, parents desert late‐season offspring when opportunities to re‐nest are absent. In these cases, any reproductive benefits of desertion are delayed, and desertion is unlikely to be advantageous unless the deserted parent can compensate for the loss of its partner and minimize costs to the current brood. We tested this parental compensation hypothesis in Hooded Warblers Setophaga citrina, a species in which males regularly desert late‐season nestlings and fledglings during moult. Females from deserted nests effectively doubled their provisioning efforts, and nestlings from deserted nests received just as much food, gained mass at the same rate, and were no more likely to die from either complete nest predation or brood reduction as young from biparental nests. The female provisioning response, however, was significantly related to nestling age; females undercompensated for male desertion when the nestlings were young, but overcompensated as nestlings approached fledging age, probably because of time constraints that brooding imposed on females with young nestlings. Overall, our results indicate that female Hooded Warblers completely compensate for male moult‐associated nest desertion, and that deserting males pay no reproductive cost for desertion, at least up to the point of fledging. Along with other studies, our findings support the general conclusion that late‐season offspring desertion is likely to evolve only when parental compensation by the deserted partner can minimize costs to the current brood.     

Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats

In cooperative animal societies, dominant females typically show higher breeding success than subordinates, and are commonly believed to control the extent of reproductive sharing. However, studies of social insect societies reveal that subordinates too can interfere with the breeding attempts of others, with important implications for the distribution of fitness within colonies. Here, we show that subordinate females in a high-skew vertebrate (the meerkat, Suricata suricatta), also exert a substantial influence over the reproductive attempts of others. In meerkat societies, pregnant dominants are known to kill subordinate litters, but we show that pregnant subordinates also kill pups; not only those of other subordinates but the dominant's as well. Litters born to females of any rank were half as likely to survive their first 4 days if a subordinate was pregnant. However, dominant females were more likely than subordinates to give birth when no other females were pregnant, and so lost fewer litters to infanticide than subordinates. This is probably due in part to dominants employing counter-tactics to reduce the incidence of subordinate pregnancy. We discuss the broad implications of subordinates having a degree of control over reproductive sharing for future attempts to understand the distribution of reproduction in animal societies.     

Reproductive sharing among queens in the ant Formica fusca

Reproductive sharing among cobreeders, in which reproductiveshares may vary from equal contribution (low reproductive skew)to reproductive dominance by one individual (high reproductiveskew), is a fundamental feature of animal societies. Recenttheoretical work, the reproductive skew models, has focusedon factors affecting the degree to which reproduction is skewedwithin a society. We used the parameters provided by skew modelsas a guideline to study determinants of reproductive sharingin polygyne ants. As a model system we used two-queen laboratorycolonies of the ant Formica fusca in which the reproductiveshares of each queen was assessed from offspring by using allozymesand DNA microsatellites. We tested how the different variablesincluded in reproductive skew models (queen-queen relatedness,potential fighting ability, productivity, and worker relatednessreflected by queen number in the colony of origin) affect reproductivesharing among queens. The results showed that the relatednessamong queens explained 26% of the variation in reproductiveskew. The size difference between queens (reflecting potentialfighting ability), colony productivity, and worker relatednessdid not have an effect on reproductive partitioning among cobreeders.To our knowledge, this is the first study to test for the effectsof various determinants of skew in an experimental setting.     

Multiple breeders, breeder shifts and inclusive fitness returns in an ant

In social insects, colonies may contain multiple reproductively active queens. This leads to potential conflicts over the apportionment of brood maternity, especially with respect to the production of reproductive offspring. We investigated reproductive partitioning in offspring females (gynes) and workers in the ant Formica fusca, and combined this information with data on the genetic returns gained by workers. Our results provide the first evidence that differential reproductive partitioning among breeders can enhance the inclusive fitness returns for sterile individuals that tend non-descendant offspring. Two aspects of reproductive partitioning contribute to this outcome. First, significantly fewer mother queens contribute to gyne (new reproductive females) than to worker brood, such that relatedness increases from worker to gyne brood. Second, and more importantly, adult workers were significantly more related to the reproductive brood raised by the colony, than to the contemporary worker brood. Thus, the observed breeder shift leads to genetic benefits for the adult workers that tend the brood. Our results also have repercussions for genetic population analyses. Given the observed pattern of reproductive partitioning, estimates of effective population size based on worker and gyne samples are not interchangeable.     

Do maternal food deprivation and offspring predator cues interactively affect maternal effort in fish?

The state of the environment parents are exposed to during reproduction can either facilitate or impair their ability to take care of their young. Thus, the environmental conditions experienced by parents can have a transgenerational impact on offspring phenotype and survival. Parental energetic needs and the variance in offspring predation risk have both been recognized as important factors influencing the quality and amount of parental care, but surprisingly, they are rarely manipulated simultaneously to investigate how parents adjust care to these potentially conflicting demands. In the maternally mouthbrooding cichlid Simochromis pleurospilus, we manipulated female body condition before spawning and exposure to offspring predator cues during brood care in a two‐by‐two factorial experiment. Subsequently, we measured the duration of brood care and the number and size of the released young. Furthermore, we stimulated females to take up their young by staged predator attacks and recorded the time before the young were released again. We found that food‐deprived females produced smaller young and engaged less in brood care behaviour than well‐nourished females. Final brood size and, related to this, female protective behaviour were interactively determined by nutritional state and predator exposure: well‐nourished females without a predator encounter had smaller broods than all other females and at the same time were least likely to take up their young after a simulated predator attack. We discuss several mechanisms by which predator exposure and maternal nutrition might have influenced brood and offspring size. Our results highlight the importance to investigate the selective forces on parents and offspring in combination, if we aim to understand reproductive strategies.     

A commitment model of reproductive inhibition in cooperatively breeding groups

Cooperatively breeding groups include individuals that giveup some current reproductive opportunities while remaining ina group. In some cases, these individuals are physiologicallyor morphologically unable to reproduce. Empirical and theoreticalevidence suggest that this inability often does not result fromstress or manipulation by dominants against the interests ofsubordinates. I argue that such reproductive inhibition canrepresent a commitment not to reproduce in exchange for a reductionin costs imposed by dominants. I present a model that allowssubordinates to choose whether to inhibit their own reproduction("self-inhibition") and accept no direct reproduction whilein the group or to remain flexible and attempt to take a shareof group productivity. If dominants assess the reproductivestatus of subordinates and punish those that reproduce, thismodel predicts self-inhibition when group members are closelyrelated, opportunities for independent breeding are poor, assessmentof reproductive status and eviction are costly, and the chanceof being detected when cheating is high. However, dominantsare less likely to assess the reproductive status of subordinatesthat are closely related, resulting in a narrow window of relatednessin which self-inhibition is favored. Counterintuitively, thiswindow is wider when flexible subordinates would be able totake a large share of group production. Although the model assumesthat dominants are able to reliably detect commitment, it isgenerally robust against mistakes in the form of dominants failingto assess uncommitted subordinates, or even low frequenciesof deception by flexible subordinates.     

Helpers at the nest improve late-life offspring performance: evidence from a long-term study and a cross-foster experiment

Background

Conditions during an individual''s rearing period can have far reaching consequences for its survival and reproduction later in life. Conditions typically vary due to variation in parental quality and/or the environment, but in cooperative breeders the presence of helpers adds an important component to this. Determining the causal effect of helpers on offspring fitness is difficult, since high-quality breeders or territories are likely to produce high-quality offspring, but are also more likely to have helpers because of past reproductive success. This problem is best resolved by comparing the effect of both helping and non-helping subordinates on offspring fitness, however species in which both type of subordinates commonly occur are rare.

Methodology/Principal Findings

We used multi-state capture-recapture models on 20 years of data to investigate the effect of rearing conditions on survival and recruitment in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), with both helping and non-helping subordinates. The number of helpers in the rearing territory, but not territory quality, group- or brood size, was positively associated with survival of offspring in their first year, and later in life. This was not a result of group size itself since the number of non-helpers was not associated with offspring survival. Furthermore, a nestling cross-foster experiment showed that the number of helpers on the pre-foster territory was not associated with offspring survival, indicating that offspring from territories with helpers do not differ in (genetic) quality.

Conclusions/Significance

Our results suggest that the presence of helpers not only increase survival of offspring in their first year of life, but also subsequent adult survival, and therefore have important fitness consequences later in life. This means that when calculating the fitness benefits of helping not only short-term but also the late-life benefits have to be taken into account to fully understand the evolution of cooperative breeding.     

Helpful Female Subordinate Cichlids Are More Likely to Reproduce

Background

In many cooperatively breeding vertebrates, subordinates assist a dominant pair to raise the dominants'' offspring. Previously, it has been suggested that subordinates may help in payment for continued residency on the territory (the ‘pay-to-stay hypothesis’), but payment might also be reciprocated or might allow subordinates access to reproductive opportunities.

Methodology/Principal Findings

We measured dominant and subordinate female alloparental brood care and reproductive success in four separate experiments and show that unrelated female dominant and subordinate cichlid fish care for each other''s broods (alloparental brood care), but that there is no evidence for reciprocal ‘altruism’ (no correlation between alloparental care received and given). Instead, subordinate females appear to pay with alloparental care for own direct reproduction.

Conclusions/Significance

Our results suggest subordinate females pay with alloparental care to ensure access to the breeding substrate and thereby increase their opportunities to lay their own clutches. Subordinates'' eggs are laid, on average, five days after the dominant female has produced her first brood. We suggest that immediate reproductive benefits need to be considered in tests of the pay-to-stay hypothesis.     

Costs of parental care on hunting behaviour of Helobdella papillornata (Euhirudinea: Glossiphoniidae)

Helobdella papillornata, an Australian freshwater leech, feeds primarily on snails and has a high level of parental care involving brooding eggs and young, with direct feeding of young. Parental costs and offspring benefits from these behaviours are poorly understood. A potential cost of parental care may be a change in the time taken to hunt prey. To test this hypothesis, the hunting behaviour of adults without progeny, parents with eggs, and parents with young were compared. We found that parents brooding eggs had a significantly (P = 0.029) longer lag time to begin hunting than parents brooding young, and spent significantly (P = 0.018) less time actively hunting than non-brooding adults. These costs, which may represent lost potential for the parent’s future reproductive success, should be outweighed by the fitness benefits of improved growth and survival of offspring, if parental care is favoured by selection. The hunting costs of care in Helobdella and other benthic, dorsoventrally flattened leeches in the family Glossiphoniidae may be smaller than the costs of brood tending that would be imposed on other freshwater leeches, and this difference may help explain the restriction of care to a single clade of the Euhirudinea.     

Reproductive skew and the threat of eviction: a new perspective

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.