Male reproductive skew, paternal relatedness, and female social relationships

Female social relationships among primates are thought to be shaped by socio-ecological factors and phylogenetic constraints. We suggest that patterns of paternal relatedness among females influence measures of social tolerance that have been used to classify species into different social relationship categories. As kin support and kin preference have only been measured for matrilineal kin and related individuals exchange less aggression and have a higher conciliatory tendency, the observed low nepotism levels and high tolerance levels may be an artifact of hidden paternal relatedness among the nonkin category. Using comparative data on macaques, we investigate this hypothesis using male reproductive skew as a proxy for paternal relatedness. Within the limitations of the study we show that populations classified as being less nepotistic, and more tolerant exhibit higher levels of reproductive skew. This first result and the reasoning behind may motivate future students of social relationships to take paternal relatedness into consideration. Potential implications of this finding if repeated with larger samples include that variation in aspects of macaque social relationships may be explained without considering phylogeny or the strength of between-group contest competition for food.     

Female preference for nests with many eggs: a cost-benefit analysis of female choice in fish with paternal care

In several fish species with paternal care, females prefer malesguarding many eggs in their nest. This preference might be advantageousbecause the presence of many other eggs dilutes the risk ofnewly laid eggs being eaten by the father. To evaluate thishypothesis quantitatively, we constructed a simulation modelthat mimics the breeding biology of the blenny Aidablenniussphynx. In contrast to earlier verbal models, the costs of choiceare explicitly taken into account We systematically varied factorssuch as the stringency of choosiness and the level and natureof the costs of choice. For realistic parameter values femalechoosiness may result in a fitness advantage of more than 50%.The optimal choice strategy created a distribution of eggs overthe nests which resembles that found in the field for A. sphynx.Our model shows that the relative fitness of a choice strategyis not constant but frequency dependent in a complicated way.If most females are choosy, a bimodal distribution of eggs overthe nests results, with many nests containing few and some nestscontaining many eggs. In such a situation choosiness is profitable,since randomly laying females will often lay their eggs in nestswith few eggs, producing a high mortality per egg due to filialcannibalism. If, on the other hand, only few choosers are present,their influence on the egg distribution is limited. A unimodaldistribution results which is profitable for nonchoosers, sincethe average egg mortality is low and nonchoosers do not bearthe costs of choice. The positive relation between chooser frequencyand chooser fitness makes it easy to understand why choosinessis evolutionarily stable. However, it is not obvious how thetrait is established by selection in the first place.[BehavEcol 7: 353–361 (1996)     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.     

Colourful traits in female birds relate to individual condition,reproductive performance and male-mate preferences: a meta-analytic approach

Colourful traits in females are suggested to have evolved and be maintained by sexual selection. Although several studies have evaluated this idea, support is still equivocal. Evidence has been compiled in reviews, and a handful of quantitative syntheses has explored cumulative support for the link between condition and specific colour traits in males and females. However, understanding the potential function of females'' colourful traits in sexual communication has not been the primary focus of any of those previous studies. Here, using a meta-analytic approach, we find that evidence from empirical studies in birds supports the idea that colourful female ornaments are positively associated with residual mass and immune response, clutch size and male-mate preferences. Hence, colourful traits in female birds likely evolved and are maintained by sexual selection as condition-dependent signals.     

The evolution of paternity and paternal care in birds

Paternity has been hypothesized to be related to the evolutionof paternal care because (1) there should be selection formales not to invest in broods with an uncertain parentage,or (2) male extrapair activity is traded against paternal care.We used interspecific comparisons to discriminate between these alternatives. Male participation in three kinds of parentalcare (nest building, incubation, provisioning of offspring)increased with high paternity in their own nests. Male parentalactivities at some stages of the breeding cycle were significantlycorrelated. A multivariate analysis taking this intercorrelationbetween different components of care and potentially confoundingvariables such as precociality, polyandry, and sexual dichromatism into account revealed that paternity was significantly positivelyrelated to offspring provisioning, while male participationin the other components of parental care did not explain asignificant amount of interspecific variation in paternity.Analyses of evolutionary transitions between different dichotomizedstates of paternity and paternal care provided no clear conclusionsconcerning evolutionary scenarios. However, theoretical arguments and the results of the contrast analyses suggest that male provisioningof offspring evolved in response to paternity.     

Evolution of paternal care in diploid and haplodiploid populations

W. D. Hamilton famously suggested that the inflated relatedness of full sisters under haplodiploidy explains why all workers in the social hymenoptera are female. This suggestion has not stood up to further theoretical scrutiny and is not empirically supported. Rather, it appears that altruistic sib‐rearing in the social hymenoptera is performed exclusively by females because this behaviour has its origins in parental care, which was performed exclusively by females in the ancestors of this insect group. However, haplodiploidy might still explain the sex of workers if this mode of inheritance has itself been responsible for the rarity of paternal care in this group. Here, we perform a theoretical kin selection analysis to investigate the evolution of paternal care in diploid and haplodiploid populations. We find that haplodiploidy may either inhibit or promote paternal care depending on model assumptions, but that under the most plausible scenarios it promotes – rather than inhibits – paternal care. Our analysis casts further doubt upon there being a causal link between haplodiploidy and eusociality.     

Year-round resource defence and the evolution of male and female song in suboscine birds: social armaments are mutual ornaments

The evolution of sexually monomorphic (i.e. mutual) ornamentation has attracted growing attention as a 'blind-spot' in evolutionary biology. The popular consensus is that female ornaments are subject to the same modes of sexual selection as males: intrasexual competition and mate choice. However, it remains unclear how these forces interact within and between sexes, or whether they fully capture selection on female traits. One possibility is that the 'armament-ornament' model - which proposes that traits used primarily in male-male contests are also co-opted by females as indicators of male quality - can be extended to explain signal evolution in both sexes. We examine this idea by testing the function of acoustic signals in two species of duetting antbirds. Behavioural observations and playback experiments suggest that male and female songs function primarily as armaments in competitive interactions. Removal experiments reveal that song is also a classic ornament used by unpaired males and females to advertise for mates. These results indicate that 'armament-ornament' processes may operate in reciprocal format, potentially explaining widespread mutual ornamentation in species with elevated intrasexual competition for resources. In addition, given that songs mediate competition between species outside the breeding season, our findings suggest that processes shaping monomorphic ornaments extend beyond the traditional definitions of sexual selection and are best understood in the broader framework of social selection.     

Male parental care, female reproductive success, and extrapair paternity

Birds differ considerably in the degree of male parental care,and it has been suggested that interspecific variation in extrapairpaternity is determined by the relative importance of benefitsto females from male parental care and good genes from extrapairsires. I estimated the relationship between extrapair paternityand the importance of male parental care for female reproductivesuccess mainly based on male removal studies, using a comparativeapproach. The reduction in female reproductive success causedby the absence of a male mate was positively correlated withthe male contribution to feeding offspring. The frequency ofextrapair paternity was negatively related to the reductionin female reproductive success caused by the absence of a mate.This was also the case when potentially confounding variablessuch as developmental mode of offspring and sexual dichromatismwere considered. A high frequency of extrapair paternity occursparticularly in bird species in which males play a minor rolein offspring provisioning and in which attractive males providerelatively little parental care. Bird species with frequentextrapair paternity thus appear to be those in which direct fitness benefits from male care are small, females can readilycompensate for the absence of male care, and indirect fitnessbenefits from extrapair sires are important.     

Comparative evidence supports a role for reproductive allocation in the evolution of female ornament diversity

1. Sexually selected ornaments are highly variable, even among closely related species, and the ultimate causes of variation in ornament evolution are unclear, including in rare cases of female ornament expression. One hypothesis is that differences across species in female reproductive allocation may help to explain patterns of female ornament expression among insects with nuptial gifts. 2. Dance flies (Diptera: Empididae: Empidinae) vary considerably among species in the presence and extravagance of female ornaments, which probably evolved through female contests for mates. In most dance flies, adult females appear to acquire all their dietary protein from nuptial gifts provided by males during mating. The importance of nuptial feeding on egg development is not yet known. 3. To test the prediction that the presence of female ornaments reflects differences in the degree to which females rely on nuptial feeding for egg development, egg development was examined in wild females of two species, one ornamented and the other unornamented. An ageing technique based on cuticular bands was validated, which permitted a regression of egg size on adult age. 4. We found that egg development depended on mating status in the ornamented species alone, meaning the eggs of unmated females of the ornamented species did not develop. This contrast across species is consistent with expectations that females of different species vary in their dependence on nuptial gifts for egg development. 5. These findings provide preliminary support for the hypothesis that differences in reproductive allocation mediate the intensity of female contests for nuptial gifts.     

Sexual selection in sticklebacks in the field: correlates of reproductive, mating, and paternal success

Male sticklebacks display multiple ornaments, and these ornamentshave been shown to be preferred by females in laboratory experiments.However, few field data exist, and it is not known whether thesepreferences are simultaneously or sequentially operative ina single population. We report correlates of reproductive successin two stickleback populations that differ in their ecology,over several periods within their breeding season. In both populationslarger males had higher reproductive success, but not in all periodsof the breeding season. Reproductive success increased withredness of the throat only in the Wohlensee population, andonly in one period that was characterized by low average success.In the Wohlensee population, the parasitic worm Pomphorhynchuslaevis is abundant, and reproductive success decreased withthe presence of the parasite. In the Roche population, maleswith nests concealed in a plant had higher mating success. Thesenests were less likely to fail, suggesting that females preferredto spawn in concealed nests because of higher offspring survivorship.The different sexual traits appear to reveal different aspectsof male quality (multiple message hypothesis): females probablyfind large males attractive because of their higher paternalquality, but it seems more likely that red males are preferred forbetter genetic qualities. Females also discriminate on territoryquality, and male traits may be important in competition forthese territories. The correlates of reproductive success werenot consistent during the season, probably due to changes inthe availability of ripe females. Such fluctuating selectionpressures will contribute to the maintenance of genetic variationin sexual traits.     

The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket

Trans‐generational immune priming is the transmission of enhanced immunity to offspring following a parental immune challenge. Although within‐generation increased investment into immunity demonstrates clear costs on reproductive investment in a number of taxa, the potential for immune priming to impact on offspring reproductive investment has not been thoroughly investigated. We explored the reproductive costs of immune priming in a field cricket, Teleogryllus oceanicus. To assess the relative importance of maternal and paternal immune status, mothers and fathers were immune‐challenged with live bacteria or a control solution and assigned to one of four treatments in which one parent, neither or both parents were immune‐challenged. Families of offspring were reared to adulthood under a food‐restricted diet, and approximately 10 offspring in each family were assayed for two measures of immunocompetence. We additionally quantified offspring reproductive investment using sperm viability for males and ovary mass for females. We demonstrate that parental immune challenge has significant consequences for the immunocompetence and, in turn, reproductive investment of their male offspring. A complex interaction between maternal and paternal immune status increased the antibacterial immune response of male offspring. This increased immune response was associated with a reduction in son's sperm viability, implicating a trans‐generational resource trade‐off between investment into immunocompetence and reproduction. Our data also show that these costs are sexually dimorphic, as daughters did not demonstrate a similar increase in immunity, despite showing a reduction in ovary mass.     

Nest ornamentation by female spotless starlings in response to a male display: an experimental study

1. The use of behavioural traits by females in signalling condition has been practically ignored in evolutionary theory. However, females may also exhibit ornaments and behavioural displays, although less elaborated than those of males. 2. In this study we suggest that the carrying of feathers by spotless starlings Sturnus unicolor Temminck females to decorate the nest represents an elaborated and costly behaviour that is displayed in response to a courtship male behaviour: the carrying of nest green plants. 3. By experimentally increasing the amount of green plants in the nests, to give the appearance that highly attractive males defended them, we induced females to increase their feather carrying rates. 4. The amount of feathers carried to the nest was correlated to female reproductive experience and laying date, two variables correlated with female body condition. These results suggests that this behaviour may work as an honest indicator of female quality. 5. We conclude that male carrying plants and female carrying feathers can be viewed as two sex-specific functionally related signalling behaviours involved in mutual courtship or status signalling.     

Symmetrical male sexual ornaments, paternal care, and offspring quality

Simultaneous manipulation of tail length and tail asymmetryin male barn swallows (Hirundo rustica) has revealed that femalesprefer maJes with both long and symmetrical tail ornaments overmales with short and asymmetrical ornaments. Fluctuating asymmetryin tail length has a negative effect on the maneuvering abilityof male barn swallows, and females may prefer males with symmetricaltail ornaments because they thereby acquire more direct fitnessbenefits in terms of paternal care. The least preferred maleswith short tails with high asymmetry performed an absolutelyand relatively larger share of feeding of nestlings than themost preferred males. However, the combined feeding rate ofthe pair was not statistically significantly different betweentreatment groups. Fully grown tarsus length and body mass ofoffspring on day 15 did not differ between treatments. Theseresults indicate that females do not prefer males with symmetricaltail ornaments because such males contribute a relatively orabsolutely larger share of parental duties. Although these resultsdo not explain the basis of female choice for long and symmetricaltails, the results are consistent with a hypothesis that femalesof species with biparental care should invest differentiallyin their offspring relative to the quality of their mates. Theresults are also consistent with a hypothesis that preferredmales have access to mates with superior parenting abilities     

Does paternity or paternal investment determine the level of paternal care and does female choice explain egg stealing in the fifteen-spined stickleback?

An earlier field study on the fifteen-spined stickleback (Spinachia spinachia) showed that frequent male—male interactionsresult in high frequencies of sneaking and egg stealing. Moreover,sneaking behavior was performed not only by males adoptingalternative mating strategies, but also by males with theirown nests. The advantage of sneaking is easily understood, but it is more difficult to explain the evolutionary benefitof stealing eggs from other males. I investigated whether malessuffering from sneaking adjust their paternal effort in relationto their degree of paternity. I also examined whether femalesprefer males that have more eggs in their nests, as this couldexplain egg stealing. There was no relationship between thedegree of paternity and fanning activity, hatching success,or nest defense. However, the older the eggs become, the morethe males increase their attack rate toward potential egg predators(goldsinny wrasse and shore crabs). Thus, males adjusted theirlevel of defense to the amount of energy and time already investedin the clutch. Females did not prefer males with more eggs intheir nests. On the contrary, females preferred males withreduced clutches over males with enlarged clutches. Therefore,female choice is unlikely to be a driving force behind eggstealing in this species.     

When assumptions on visual system evolution matter: nestling colouration and parental visual performance in birds

Comparative studies in visual ecology of birds often rely on several assumptions on the evolution of avian vision. In this study, we show that when these assumptions are not upheld, conclusions may be strongly affected. To illustrate this purpose, we reanalysed the data of Avilés & Soler (J. Evol. Biol. 22 : 376–386, 2009) who demonstrated that nestling gape colouration in altricial birds is associated with visual system. We show that a slight change in analysis methodology leads to opposite conclusions. Such conflicting result raises the problem of applying powerful methods developed for continuous variables to a small sample and a small number of independent events of qualitative visual system shift in comparative analyses. Further, we show that the current trend to assume strong phylogenetic inertia of avian visual systems is contradicted by data and that the sequencing of the SWS1 opsin gene should be considered as an alternative approach.     

The unexpected but understandable dynamics of mating,paternity and paternal care in the ocellated wrasse

Although theory generally predicts that males should reduce paternal care in response to cues that predict increased sperm competition and decreased paternity, empirical patterns are equivocal. Some studies have found the predicted decrease in male care with increased sperm competition, while even more studies report no effect of paternity or sperm competition on male care. Here, we report the first example, to our knowledge, of paternal care increasing with the risk and intensity of sperm competition, in the ocellated wrasse (Symphodus ocellatus). Theory also predicts that if paternal care varies and is important to female fitness, female choice among males and male indicators traits of expected paternal care should evolve. Despite a non-random distribution of mating success among nests, we found no evidence for female choice among parental males. Finally, we document the highest published levels of extra-pair paternity for a species with exclusive and obligate male care: genetic paternity analyses revealed cuckoldry at 100 per cent of nests and 28 per cent of all offspring were not sired by the male caring for them. While not predicted by any existing theory, these unexpected reproductive patterns become understandable if we consider how male and female mating and parental care interact simultaneously in this and probably many other species.     

Do egg size and parental care coevolve in fishes?

A phenomenon that has attracted a substantial theoretical and empirical interest is the positive relationship between egg size and the extent of parental care in fishes. Interestingly, despite the effort put into solving the causality behind this relationship over the past two decades it remains largely unsolved. Moreover, how general the positive relationship between egg size and parental care is among fishes is also poorly understood. In order to stimulate research exploring egg size and parental care variation in fishes, the potential selective forces from both natural and sexual selection on egg size and parental care are discussed. Recent empirical findings on how oxygen requirements and developmental times may differ between differently sized eggs are incorporated into a critical view of the current theory of this field. Furthermore, it is suggested that the up to now neglected effects of sexual selection, through both mate choice and sexual conflict, can have strong effects on the relationship between egg size and parental care in fishes. In light of the recent developments of comparative and experimental methods, future approaches that may improve the understanding of the relationship between egg size and care in fishes are suggested.