Parental investment, sexual selection and sex ratios

Conventional sex roles imply caring females and competitive males. The evolution of sex role divergence is widely attributed to anisogamy initiating a self‐reinforcing process. The initial asymmetry in pre‐mating parental investment (eggs vs. sperm) is assumed to promote even greater divergence in post‐mating parental investment (parental care). But do we really understand the process? Trivers [Sexual Selection and the Descent of Man 1871–1971 (1972), Aldine Press, Chicago] introduced two arguments with a female and male perspective on whether to care for offspring that try to link pre‐mating and post‐mating investment. Here we review their merits and subsequent theoretical developments. The first argument is that females are more committed than males to providing care because they stand to lose a greater initial investment. This, however, commits the ‘Concorde Fallacy’ as optimal decisions should depend on future pay‐offs not past costs. Although the argument can be rephrased in terms of residual reproductive value when past investment affects future pay‐offs, it remains weak. The factors likely to change future pay‐offs seem to work against females providing more care than males. The second argument takes the reasonable premise that anisogamy produces a male‐biased operational sex ratio (OSR) leading to males competing for mates. Male care is then predicted to be less likely to evolve as it consumes resources that could otherwise be used to increase competitiveness. However, given each offspring has precisely two genetic parents (the Fisher condition), a biased OSR generates frequency‐dependent selection, analogous to Fisherian sex ratio selection, that favours increased parental investment by whichever sex faces more intense competition. Sex role divergence is therefore still an evolutionary conundrum. Here we review some possible solutions. Factors that promote conventional sex roles are sexual selection on males (but non‐random variance in male mating success must be high to override the Fisher condition), loss of paternity because of female multiple mating or group spawning and patterns of mortality that generate female‐biased adult sex ratios (ASR). We present an integrative model that shows how these factors interact to generate sex roles. We emphasize the need to distinguish between the ASR and the operational sex ratio (OSR). If mortality is higher when caring than competing this diminishes the likelihood of sex role divergence because this strongly limits the mating success of the earlier deserting sex. We illustrate this in a model where a change in relative mortality rates while caring and competing generates a shift from a mammalian type breeding system (female‐only care, male‐biased OSR and female‐biased ASR) to an avian type system (biparental care and a male‐biased OSR and ASR).     

Sexual selection and extrapair fertilization in a socially monogamous passerine, the zebra finch (Taeniopygia gullata)

We investigated paternal exclusion rate (the percentage of youngreared by a male that were not his genetic offspring), and behavioraland reproductive variables influencing this rate, in a freelybreeding laboratory population of zebra finches (Tae-niopygiaguttala castanotis), a socially monogamous grassfinch. Priorto the experiment, each male founder was fitted with eithertwo red bands (creating a phenotype previously demonstratedto be attractive to females) or two green bands (unattractiveto females) as part of a unique combination of four leg bands.The overall paternal exclusion rate was 28%, as determined bymultilocus, minisatellite DNA fingerprinting of 278 offspringreared by 26 males and their mates. Mean exclusion rates were16% and 40% for red- and green-banded males, respectively. Exclusionrates were directly proportional to rates of female participationin unforced extrapair copulations (UEPCs) with red-banded malesthat occurred when females were fertile. Rates of fertile, forcedextrapair copulations (FEPCs) and fertile UEPCs involving green-bandedmales either failed to influence exclusion rate or varied inverselywith exclusion rate, indicating that extrapair fertilization(EPF) is under female control. Effort devoted by males to seekingEPFs increased exclusion rate. Results suggest that males placegreater effort into seeking fertile versus infertile EPCs andthat unattractive males accrue fitness gains through high parentalinvestment (PI), whereas attractive males benefit through decreasedPI and increased allocation to EPF.     

Sex allocation in response to paternal attractiveness in the zebra finch

Females mated to attractive males are predicted to produce male-biasedbroods. Previous studies on zebra finches, Taeniopygia guttata,in which colored leg rings were used to alter male attractiveness,support this hypothesis. However, because molecular sexing techniqueswere not available, it was not known when during developmentthis bias arose. Also, because both attractive (red-ringed)and unattractive (green-ringed) males were within the same aviary,assortative mating between treatments may have confounded theresults. Using two different experimental designs, we testedwhether the sex ratio of zebra finch eggs and chicks differedin response to paternal ring color whilst controlling for assortativemating between treatments. In the aviary experiment, birds couldinteract socially, but all males in an aviary had the same legring color. In the cage experiment, each female was randomlyassigned a red- or green-ringed mate, thus also eliminatingassortative mating within treatments. Offspring were sexed basedon plumage or using a molecular method. The sex ratio at layingdid not differ between treatments in either the aviary (n =313 eggs) or cage (n = 151 eggs) experiments, suggesting thatfemale zebra finches do not manipulate the primary sex ratioin response to their mate's ring color. However, in the cageexperiment we found greater male embryonic mortality in theattractive group, which resulted in a female-biased sex ratioat sexual maturity, that is, in the opposite direction to thatfound in previous studies. Possible explanations for the disparitybetween our results and those of previous studies are considered.     

Sex-specific growth rates in zebra finch nestlings: a possible mechanism for sex ratio adjustment

Wild and captive zebra finches (Taenopygia guttata), like severalother species, produce a male-biased sex ratio at fledging whenfood is scarce. This is due to primary sex-ratio adjustmentand female-biased nestling mortality. Given that young femalesfledging at low body masses have been shown to have low fecundityas adults, lower returns to parents from producing female offspringin conditions of restricted food has been raised as a functionalexplanation (Trivers and Willard's hypothesis of adaptive sexualinvestment; 1973). However, an alternative, mechanistic hypothesisis that under restricted conditions female chicks are more costlyto produce. In consequence, lower returns to parents under theseconditions would happen earlier in the life of female offspringrather than later. To test this hypothesis, I hand-reared chickson a food gradient. In the absence of parent-offspring and sib-sibinteractions, final body mass and growth rates for females werelower in conditions of restricted food. For males, final bodymass and growth rates did not differ with food condition. Lowfemale growth rates in food-restricted conditions might be onepotential mechanism causing female-biased mortality in birds.More importantly, this result is the strongest evidence yetof female offspring experiencing higher marginal fitness benefitsfrom additional food than males and it has implications forprimary and secondary sex-ratio adjustment. Also, as this mechanismhas been shown in the absence of parent-offspring interactions,significant questions can now be raised as to how parental andoffspring behavior interact in their effects on secondary sex-ratioadjustment.     

Extrapair paternity and the opportunity for sexual selection in a socially monogamous passerine

Effects of alternate mating strategies on the opportunity forsexual selection are widely debated, and recent studies haveconcluded that the effects of extrapair (EP) paternity on theopportunity for sexual selection may have been overstated dueto 1) methodological limitations of empirical studies and 2)the potential for males to gain from additional within-pair(WP) reproductive opportunities. We therefore examined the impactof EP paternity on the opportunity for sexual selection in thesocially monogamous and single-brooded eastern kingbird (Tyrannustyrannus). EP paternity was common in all 3 years of our study(61% of 89 broods, 47% of nestlings) and realized reproductivesuccess (EP + WP young) ranged from 0 to 9 young/male/year.A total of 31% of males lost all WP paternity (24% sired neitherWP nor EP young, whereas 7% sired EP but not WP young), andvariance in male realized reproductive success was more than9 times greater than that of apparent reproductive success.Nearly half of EP mates were not nearest neighbors, and manywere separated by 3 or more territories (>1000 m). EP successwas independent of nest defense behavior, but early singingmales and males with high song rates were most successful atboth a population level and when cuckolders and cuckoldees werecompared. EP paternity contributed significantly to the opportunityfor sexual selection in kingbirds, and we suggest that thisis probably due to the low potential for WP variation in reproductivesuccess, apparent long-distance movements of one or both sexes,and consequent absence of reciprocal cuckoldry.     

Nest building, sexual selection and parental investment

Avian nest building has traditionally been viewed as resulting in natural selection advantages, but it is also been associated with courtship and pair formation. We hypothesize that nest-building activity could be used as a sexually selected display, allowing each sex to obtain reliable information on the condition of the other. In this paper, we test the ‘good parent’ process in a scenario where nest size is a sexually selected trait. Thus, individuals with more extreme displays (larger nests) might obtain benefits in terms of either parental investment or differential parental investment by the partner. We predicted that: (1) species in which both sexes contribute to nest building have larger nests than those in which the nest is built only by one sex, because both sexes are using the nest-building process as a signal of their quality; (2) species in which both sexes work together in the nest-building process invest more in reproduction, because each can assess the other more reliably than in species where only one sex participates in nest building; and (3) in light of the two preceding predictions, nest size should be positively related to investment in parental care. A comparative analysis of 76 passerine species confirmed that nest size, relative to the species' body size, is larger when both sexes build the nest and that species with a larger nest relative to their body size invest more in reproduction. This revised version was published online in July 2006 with corrections to the Cover Date.     

Sex-biased survival predicts adult sex ratio variation in wild birds

Adult sex ratio (ASR) is a central concept in population demography and breeding system evolution, and has implications for population viability and biodiversity conservation. ASR exhibits immense interspecific variation in wild populations, although the causes of this variation have remained elusive. Using phylogenetic analyses of 187 avian species from 59 families, we show that neither hatching sex ratios nor fledging sex ratios correlate with ASR. However, sex-biased adult mortality is a significant predictor of ASR, and this relationship is robust to 100 alternative phylogenetic hypotheses, and potential ecological and life-history confounds. A significant component of adult mortality bias is sexual selection acting on males, whereas increased reproductive output predicts higher mortality in females. These results provide the most comprehensive insights into ASR variation to date, and suggest that ASR is an outcome of selective processes operating differentially on adult males and females. Therefore, revealing the causes of ASR variation in wild populations is essential for understanding breeding systems and population dynamics.     

Evolution of displays within the pair bond

Although sexual selection is an important cause of display evolution, in socially monogamous species (e.g. many birds), displays continue after formation of the pair bond. Here, we consider that these displays evolve because they stimulate the partner to increase investment in offspring. Our study is motivated by elaborate mutual displays in species that are largely monomorphic and have long-term pair bonds (e.g. the great crested grebe, Podiceps cristatus) and by many empirical results evidencing that display manipulation affects parental investment. Using population genetic models, we show that a necessary condition for the permanent establishment of mutual displays in the pair bond is that the benefit of investment by the pair is more than twice that resulting from investment by a single individual. Pre-existing biases to respond to displays by increased investment are a necessary component of display evolution. We also consider examples where one sex (e.g. males) stimulates increased investment in offspring by the other sex. Here, display and additional investment cannot evolve permanently, but can increase and linger at high frequency for a long time before loss. We discuss how such transient effects may lead to the evolution of permanent displays as a result of evolution at additional loci.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

Ecological gradient of sexual selection: elevation and song elaboration in finches

Ecological gradients in natural and sexual selection often result in evolutionary diversification of morphological, life history, and behavioral traits. In particular, elevational changes in habitat structure and climate not only covary with intensity of sexual selection in many taxa, but may also influence evolution of mating signals. Here we examined variation in courtship song in relation to elevation of breeding across cardueline finches-a subfamily of birds that occupies the widest elevational range of extant birds and shows extensive variation in life histories and sexual selection along this range. We predicted that decrease in sexual selection intensity with elevation of breeding documented in this clade would result in a corresponding evolutionary reduction in elaboration of courtship songs. We controlled for the effects of phylogeny, morphology, and habitat structure to uncover a predicted elevational decline in courtship song elaboration; species breeding at lower elevations sang more elaborated and louder songs compared to their sister species breeding at higher elevations. In addition, lower elevation species had longer songs with more notes, whereas frequency components of song did not vary with elevation. We suggest that changes in sexual selection account for the observed patterns of song variation and discuss how elevational gradient in sexual selection may facilitate divergence in mating signals potentially reinforcing or promoting speciation.     

Adult sex ratio,sexual dimorphism and sexual selection in a Mesozoic reptile

The evolutionary history of sexual selection in the geologic past is poorly documented based on quantification, largely because of difficulty in sexing fossil specimens. Even such essential ecological parameters as adult sex ratio (ASR) and sexual size dimorphism (SSD) are rarely quantified, despite their implications for sexual selection. To enable their estimation, we propose a method for unbiased sex identification based on sexual shape dimorphism, using size-independent principal components of phenotypic data. We applied the method to test sexual selection in Keichousaurus hui, a Middle Triassic (about 237 Ma) sauropterygian with an unusually large sample size for a fossil reptile. Keichousaurus hui exhibited SSD biased towards males, as in the majority of extant reptiles, to a minor degree (sexual dimorphism index −0.087). The ASR is about 60% females, suggesting higher mortality of males over females. Both values support sexual selection of males in this species. The method may be applied to other fossil species. We also used the Gompertz allometric equation to study the sexual shape dimorphism of K. hui and found that two sexes had largely homogeneous phenotypes at birth except in the humeral width, contrary to previous suggestions derived from the standard allometric equation.     

Sex allocation and sexual conflict in simultaneously hermaphroditic animals

Links between sex allocation (SA) and sexual conflict in simultaneous hermaphrodites have been evident since Charnov''s landmark paper published 30 years ago. We discuss two links, namely the potential for sexual conflict over SA between sperm donor and recipient, and the importance of post-copulatory sexual selection and the resulting sexual conflict for the evolution of SA. We cover the little empirical and theoretical work exploring these links, and present an experimental test of one theoretical prediction. The link between SA and sexual conflict is an interesting field for future empirical and theoretical research.     

Strategic egg allocation in the zebra fish, Danio rerio

Females across a range of taxa have been shown to differentiallyallocate their reproductive resources according to the attractivenessof their mate. Previous studies demonstrated a female preferencefor larger males in the zebra fish but have so far failed touncover a size-mediated difference in male mating success, possiblydue to the effects of male–male competition. By controllingfor male–male competition in the present study, we showthat females strategically allocate their reproductive resources(i.e., eggs) toward larger males. When females were mated sequentiallywith a large and small male, they released a greater numberof eggs to the second male when he was large than when he wassmall. Furthermore, there was also a trend for females to releasea greater proportion of their eggs to the first male when hewas large. Across females, the total number of eggs laid byeach female increased with the average standard length of themale pair, whereas the number of eggs laid to the second malealso increased with his standard length. This study representsone of the first attempts at identifying differential allocationin a resource-free egg scatterer and suggests that female preferencesmay play a greater role in the reproductive success of malesin this species than previously envisaged.     

Predicting the direction of sexual selection

Our current understanding of the operation of sexual selection is predicated on a sex difference in parental investment, which favours one sex becoming limiting and choosy over mates, the other competitive and nonchoosy. This difference is reflected in the operational sex ratio (OSR), the ratio of sexually receptive males to females, considered to be of fundamental importance in predicting the direction of sexual selection. Difficulties in measuring OSR directly have led to the use of the potential reproductive rates (PRR) as a measure of the level of investment in offspring of males and females. Several recent studies have emphasized that other factors, such as variation in mate quality and sex differences in mortality patterns, also influence the direction of sexual selection. However, as yet there has been no attempt to form a comprehensive theory of sex roles. Here we show that neither OSR nor PRR is the most fundamentally important determinant of sex roles, and that they are not interchangeable. Instead, the cost of a single breeding attempt has a strong direct effect on competition and choosiness as well as consistent relationships to both OSR and PRR. Our life history based approach to mate choice also yields simple, testable predictions on lack of choice in either sex and on mutual mate choice.     

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     

When mothers make sons sexy: maternal effects contribute to the increased sexual attractiveness of extra-pair offspring

Quality differences between offspring sired by the social and by an extra-pair partner are usually assumed to have a genetic basis, reflecting genetic benefits of female extra-pair mate choice. In the zebra finch (Taeniopygia guttata), we identified a colour ornament that is under sexual selection and appears to have a heritable basis. Hence, by engaging in extra-pair copulations with highly ornamented males, females could, in theory, obtain genes for increased offspring attractiveness. Indeed, sons sired by extra-pair partners had larger ornaments, seemingly supporting the genetic benefit hypothesis. Yet, when comparing ornament size of the social and extra-pair partners, there was no difference. Hence, the observed differences most likely had an environmental basis, mediated, for example, via differential maternal investment of resources into the eggs fertilized by extra-pair and social partners. Such maternal effects may (at least partly) be mediated by egg size, which we found to be associated with mean ornament expression in sons. Our results are consistent with the idea that maternal effects can shape sexual selection by altering the genotype-phenotype relationship for ornamentation. They also caution against automatically attributing greater offspring attractiveness or viability to an extra-pair mate's superior genetic quality, as without controlling for differential maternal investment we may significantly overestimate the role of genetic benefits in the evolution of extra-pair mating behaviour.