The evolution of sexual dimorphism in parasitic cuckoos: sexual selection or coevolution?

Sexual dimorphism is ubiquitous in animals and can result from selection pressure on one or both sexes. Sexual selection has become the predominant explanation for the evolution of sexual dimorphism, with strong selection on size-related mating success in males being the most common situation. The cuckoos (family Cuculidae) provide an exceptional case in which both sexes of many species are freed from the burden of parental care but where coevolution between parasitic cuckoos and their hosts also results in intense selection. Here, we show that size and plumage differences between the sexes in parasitic cuckoos are more likely the result of coevolution than sexual selection. While both sexes changed in size as brood parasitism evolved, we find no evidence for selection on males to become larger. Rather, our analysis indicates stronger selection on parasitic females to become smaller, resulting in a shift from dimorphism with larger females in cuckoos with parental care to dimorphism with larger males in parasitic species. In addition, the evolution of brood parasitism was associated with more cryptic plumage in both sexes, but especially in females, a result that contrasts with the strong plumage dimorphism seen in some other parasitic birds. Examination of the three independent origins of brood parasitism suggests that different parasitic cuckoo lineages followed divergent evolutionary pathways to successful brood parasitism. These results argue for the powerful role of parasite-host coevolution in shaping cuckoo life histories in general and sexual dimorphism in particular.     

Reversed sexual size dimorphism and parental care in the Red-footed Booby Sula sula

The 'division-of-labour' hypothesis predicts that males and females perform different roles in parental care and that natural selection acts differently on each sex so as to produce different body size optima suited to their particular roles. Reversed sexual size dimorphism in avian species (females larger than males) may therefore be an adaptive consequence of different roles of males and females in parental care. We investigated patterns of nest attendance, brooding, foraging and provisioning rate in a tropical seabird, the Red-footed Booby Sula sula , a species showing a reversed sexual size dimorphism. During incubation, females attended the nest more often than males, and spent more time brooding the small chick than did males during daytime. Males and females did not differ in the average duration of their foraging trips. During incubation, there was a positive relationship between nest attendance and the duration of foraging trips in males, but not in females. During the small-chick stage, for the same time spent at the nest, males spent significantly more time than females at sea. On average, females fed the chick more often than did males. In males, there was a significant and positive relationship between the probability of feeding the chick and the duration of the foraging trip, whereas in females, this probability was much less dependent on the duration of the foraging trip. Overall, female Red-footed Boobies achieved slightly, but significantly, more parental commitment than did males. However, these sexual differences in parental participation were small, suggesting a minimal division of labour in the Red-footed Booby. Our results suggest that the division of labour hypothesis is unlikely to explain fully the adult size dimorphism in Red-footed Boobies.     

Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection

Abstract. Charadrii (shorebirds, gulls, and alcids) have an unusual diversity in their sexual size dimorphism, ranging from monomorphism to either male-biased or female-biased dimorphism. We use comparative analyses to investigate whether this variation relates to sexual selection through competition for mates or natural selection through different use of resources by males and females. As predicted by sexual selection theory, we found that in taxa with socially polygynous mating systems, males were relatively larger than females compared with less polygynous species. Furthermore, evolution toward socially polyandrous mating systems was correlated with decreases in relative male size. These patterns depend on the kinds of courtship displays performed by males. In taxa with acrobatic flight displays, males are relatively smaller than in taxa in which courtship involves simple flights or displays from the ground. This result remains significant when the relationship with mating system is controlled statistically, thereby explaining the enigma of why males are often smaller than females in socially monogamous species. We did not find evidence that evolutionary changes in sexual dimorphism relate to niche division on the breeding grounds. In particular, biparental species did not have greater dimorphism in bill lengths than uniparental species, contrary to the hypothesis that selection for ecological divergence on the breeding grounds has been important as a general explanation for patterns of bill dimorphism. Taken together, these results strongly suggest that sexual selection has had a major influence on sexual size dimorphism in Charadrii, whereas divergence in the use of feeding resources while breeding was not supported by our analyses.     

Ecological factors regulating brood attendance patterns of the Western Sandpiper Calidris mauri

Parental brood attendance patterns vary greatly among shorebird species. For monogamous calidridine species, biparental care with female-first brood departure is most common. It is believed that adult sandpipers balance potential individual survival costs associated with extended parental care against the benefit gained by their brood of prolonged parental care. These costs and benefits are difficult to quantify and factors affecting the termination of parental brood attendance are unclear. We compared clutch size, nesting phenology, and parental attendance patterns of Western Sandpipers Calidris mauri at Nome and Kanaryarmiut, Alaska, sites separated by three degrees of latitude. The sites differed in breeding density and duration of breeding season, but the distribution of clutch sizes did not differ between sites or between nesting attempts. Parental attendance patterns were similar between sites, suggesting that parental attendance is a highly conserved life-history trait in Western Sandpipers. Male Western Sandpipers attended broods longer than females, and the duration of parental attendance decreased at a similar rate for both sexes as the season progressed. Male and female Western Sandpipers undertake differential migrations to their non-breeding grounds, with males typically settling at more northerly locations and females at more southerly sites, a migration pattern shared by certain other monogamous calidridine species. These same species exhibit similar parental brood attendance patterns, suggesting the strong role of overall migration distance in shaping the expression of parental attendance behaviours. A contrast of more geographically disjunct sites coupled with a better understanding of the migratory connectivity between Western Sandpiper breeding and non-breeding populations would elucidate the role of cross-seasonal effects on parental brood attendance decisions.     

Sexual size monomorphism in the crested porcupine (Hystrix cristata)

Amongst mammals, female-biased sexual size dimorphism (SSD) is rare and it occurs mostly in species where reduced male intrasexual competition is present. Reverse SSD has been reported for Old World porcupines Hystrix spp. We compared weight and six metric body measurements of 40 male and 42 female crested porcupines from Southern Tuscany, Italy. No significant difference was observed between sexes. The monogamous mating system of porcupines, sharing parental care, together with no evidence of territoriality, militate against previous claims of SSD presence, probably due to small sample size and inappropriate statistical analyses.     

Sexual size dimorphism and reproductive ecology in relation to mating system in waders

The relationship between sexual size dimorphism, body-weight and different reproductive traits (e.g. clutch size, egg weight and incubation period) in relation to mating system and forms of parental care was studied in waders. Two hypotheses were examined. (1) Sexual size dimorphism is correlated with the intensity of sexual selection. (2) The degree of sexual size dimorphism is the result of an interrelationship between the reproductive strategy of the female and her body size. In the polygynous species the male was significantly larger than the female. This is consistent with the sexual selection hypothesis. However, among waders, a positive correlation exists between egg weight, clutch mass and body-weight. Selection for small eggs or a short incubation period may therefore have an influence on female body-weight. If the lack of paternal care reduces the female's possibility for producing large eggs or incubating a large clutch mass, we would expect a selection pressure for small female size among polygynous species. Thus, large sexual size dimorphism among polygynous waders may be a result of selection for small female size to lack of paternal care, or selection for large male size due to intramale competition or a female preference for large-sized males. In multiple-clutch species (viz. species in which the female regularly lays more than one clutch during the season) egg weight was low both for a given female and male body-weight. The low egg weight of multiple-clutch species is assumed to be a result of the constraints placed on the female from producing several clutches during a single breeding season.     

Limited male incubation ability and the evolution of egg size in shorebirds

In bird species where males incubate but are smaller than females, egg size may be constrained by male body size, and hence ability to incubate the eggs. Using data from 71 such shorebird species, we show that egg size decreases as the degree of female-biased sexual size dimorphism increases, after controlling for female body mass. Relative egg size was not related to mean clutch size. However, when controlling for mating system, the relationship between female-biased sexual size dimorphism and relative egg size was only significant in polyandrous species. The relatively small eggs of socially polyandrous shorebirds have previously been explained as an energy-saving strategy associated with the production of multiple clutches. Our findings suggest that egg size evolution is better explained by male incubation limitation in these birds.     

Comparative analyses of the influence of developmental mode on phenotypic diversification rates in shorebirds

Phenotypic diversity is not evenly distributed across lineages. Here, we describe and apply a maximum-likelihood phylogenetic comparative method to test for different rates of phenotypic evolution between groups of the avian order Charadriiformes (shorebirds, gulls and alcids) to test the influence of a binary trait (offspring demand; semi-precocial or precocial) on rates of evolution of parental care, mating systems and secondary sexual traits. In semi-precocial species, chicks are reliant on the parents for feeding, but in precocial species the chicks feed themselves. Thus, where the parents are emancipated from feeding the young, we predict that there is an increased potential for brood desertion, and consequently for the divergence of mating systems. In addition, secondary sexual traits are predicted to evolve faster in groups with less demanding young. We found that precocial development not only allows rapid divergence of parental care and mating behaviours, but also promotes the rapid diversification of secondary sexual characters, most notably sexual size dimorphism (SSD) in body mass. Thus, less demanding offspring appear to facilitate rapid evolution of breeding systems and some sexually selected traits.     

Brood desertion by female shorebirds: a test of the differential parental capacity hypothesis on Kentish plovers.

The aim of this study was to examine whether the energetic costs of reproduction explain offspring desertion by female shorebirds, as is suggested by the differential parental capacity hypothesis. A prediction of the hypothesis is that, in species with biparental incubation in which females desert from brood care after hatching, the body condition of females should decline after laying to a point at which their body reserves are too low for continuing parental care. We tested this prediction on Kentish plovers (Charadrius alexandrinus) in which both sexes incubate but the females desert from brood care before the chicks fledge. We found no changes in either the body masses or body compositions of both individual male and female plovers from early incubation and throughout early chick rearing. Furthermore, the timing of brood desertion by females was not affected by their body condition. Neither did we find gender differences in the energetic costs of incubation. There were no differences in the timing of brood desertion between experimental and control females in an experiment in which we lengthened or shortened the duration of incubation by one week. These results indicate that energetic costs do not explain offspring desertion by female Kentish plovers and that the needs of chicks for parental care rather than cumulative investment by females is what determines the timing of brood desertion.     

The evolution of fecundity is associated with female body size but not female‐biased sexual size dimorphism among frogs

Sexual size dimorphism (SSD) is one of the most common ways in which males and females differ. Male‐biased SSD (when males are larger) is often attributed to sexual selection favouring large males. When females are larger (female‐biased SSD), it is often argued that natural selection favouring increased fecundity (i.e. larger clutches or eggs) has coevolved with larger female body size. Using comparative phylogenetic and multispecies regression model selection approaches, we test the hypothesis that among‐species variation in female fecundity is associated with the evolution of female‐biased SSD. We also ask whether the hypothesized relationship between SSD and fecundity is relaxed upon the evolution of parental care. Our results suggest a strong relationship between the evolution of fecundity and body size, but we find no significant relationship between fecundity and SSD. Similarly, there does not appear to be a relationship between fecundity and the presence or absence of parental care among species. Thus, although female body size and fecundity coevolve, selection for increased fecundity as an explanation for female‐biased SSD is inconsistent with our analyses. We caution that a relationship between female body size and fecundity is insufficient evidence for fecundity selection driving the evolution of female‐biased SSD.     

Post-fledging brood and care division in the roseate tern (Sterna dougallii)

Extended post-fledging parental care is an important aspect of parental care in birds, although little studied due to logistic difficulties. Commonly, the brood is split physically (brood division) and/or preferential care is given to a subset of the brood by one parent or the other (care division). Among gulls and tern (Laridae), males and females generally share parental activities during the pre-fledging period, but the allocation of parental care after fledging is little documented. This study examined the behaviour of male and female roseate terns (Sterna dougallii) during the late chick-rearing and early post-fledging periods, and in particular the amount of feeds and the time spent in attendance given to individual chicks/fledglings. Pre-fledging parental care was biparental in all cases. Post-fledging parental care was dependent on the number of fledglings in the brood. Males and females continued biparental care in clutches with one surviving fledgling, while in two-fledgling clutches, males fed the A-fledgling while females fed the B-fledgling. Overall, there was no difference in attendance, only in feeds. This division of care may be influenced by the male only being certain of the paternity of the A-chick but not by chick sex.     

Do polyandrous shorebirds trade off egg size with egg number?

Classical polyandry in birds is rare and is most frequent in the shorebirds (Charadriiformes). Polyandrous shorebirds lay smaller eggs for their body masses than non-polyandrous shorebirds, indicating that polyandrous female shorebirds may trade egg size off against number of eggs in order to maximize reproductive success. However, this trade-off may be confounded by phylogeny because most polyandrous species belong to a single family, the Jacanidae. I re-analysed this adaptive hypothesis using phylogenetically-independent contrast analyses. These analyses showed that there was no statistically significant difference in egg size between polyandrous and monogamous shorebirds once the effects of phylogeny had been incorporated. This is one of the first studies to show that the results of independent contrasts analyses differ from those where phylogenetic effects have not been taken into account.     

Maternal nutritional condition and genetic differentiation affect brood size and offspring body size in Nicrophorus

In most animal species, brood size and body size exhibit some variation within and between populations. This is also true for burying beetles (genus Nicrophorus), a group in which the body size of offspring depends critically on the number of offspring competing for food due to the discrete nature of resource used for larval nutrition (vertebrate carcasses). In one species, brood size and body size are correlated with population density, and appear to be phenotypically plastic. We investigated potential proximate causes of between-population variation in brood size and body size in two species, Nicrophorus vespilloides and Nicrophorus defodiens. Our first experiment supported the notion that brood size is phenotypically plastic, because it was affected by environmental variation in adult nutritional condition. We found that the pre-breeding nutritional status of female N. vespilloides affected the number of eggs they laid, the number of surviving larvae in their broods, and the body size of their offspring. We do not know whether this plasticity is adaptive because greater offspring body size confers an advantage in contests over breeding resources, or whether starved females are constrained to produce smaller clutches because they cannot fully compensate for their poor pre-breeding nutritional status by feeding from the carcass. Our second experiment documents that brood size, specifically the infanticidal brood-size adjustment behavior, has undergone genetic differentiation between two populations of N. defodiens. Even under identical breeding conditions with identical numbers of first-instar larvae, females descended from the two populations produced broods of different size with corresponding differences in offspring body size.     

Sexual size dimorphism in red-necked phalaropes and functional significance of nonsexual bill structure variation for feeding performance

Sexual size dimorphism is widespread in shorebirds, yet no tests of the assumption that such size dimorphism extends to functionally significant dimensions of the bill exist. This report presents tests of: (1) the assumption that sexual size dimorphism extends to the feeding structures in sexually size dimorphic bird, and (2) the hypothesis that bill-size variation influences feeding performance in Phalaropus lobatus, the red-necked phalarope. Discriminant function analysis revealed that the sexes of this species can be distinguished on the basis of five body size/bill length variables, but with low accuracy in sexing of females because of misclassification of small females as males. In the shorebird literature, the assumption is generally made that in the absence of selection to the contrary, bill size scales to body size and hence sexual size dimorphism extends to bill size. However, discriminant function analysis of measures from red-necked phalaropes failed to separate the sexes on the basis of either external or internal bill dimensions other than length. Nonetheless, internal dimensions of the upper jaw combined with exposed culmen length explained 86% of the variance in feeding performance of phalaropes; high feeding performance depends on a wide, shallow, complex internal bill structure. This study provides evidence that internal bill dimensions determine feeding performance in a manner consistent with the mechanics of surface tension transport of prey. These results suggest that some dimensions of bill size may be constrained by performance demands and demonstrate that variation in bill morphology has functional consequences. © 1996 Wiley-Liss, Inc.     

Development of intraspecific size variation in black coucals,white-browed coucals and ruffs from hatching to fledging

Most studies on sexual size dimorphism address proximate and functional questions related to adults, but sexual size dimorphism usually develops during ontogeny and developmental trajectories of sexual size dimorphism are poorly understood. We studied three bird species with variation in adult sexual size dimorphism: black coucals (females 69% heavier than males), white-browed coucals (females 13% heavier than males) and ruffs (males 70% heavier than females). Using a flexible Bayesian generalized additive model framework (GAMM), we examined when and how sexual size dimorphism developed in body mass, tarsus length and bill length from hatching until fledging. In ruffs, we additionally examined the development of intrasexual size variation among three morphs (Independents, Satellites and Faeders), which creates another level of variation in adult size of males and females. We found that 27–100% of the adult inter- and intrasexual size variation developed until fledging although none of the species completed growth during the observational period. In general, the larger sex/morph grew more quickly and reached its maximal absolute growth rate later than the smaller sex/morph. However, when the daily increase in body mass was modelled as a proportion, growth patterns were synchronized between and within sexes. Growth broadly followed sigmoidal asymptotic models, however only with the flexible GAMM approach, residual distributions were homogeneous over the entire observation periods. These results provide a platform for future studies to relate variation in growth to selective pressures and proximate mechanisms in these three species, and they highlight the advantage of using a flexible model approach for examining growth variation during ontogeny.     

Relationship between reversed sexual dimorphism,breeding investment and foraging ecology in a pelagic seabird,the masked booby

Reversed sexual dimorphism (RSD) may be related to different roles in breeding investment and/or foraging, but little information is available on foraging ecology. We studied the foraging behaviour and parental investment by male and female masked boobies, a species with RSD, by combining studies of foraging ecology using miniaturised activity and GPS data loggers of nest attendance, with an experimental study where flight costs were increased. Males attended the chick more often than females, but females provided more food to the chick than males. Males and females foraged during similar periods of the day, had similar prey types and sizes, diving depths, durations of foraging trips, foraging zones and ranges. Females spent a smaller proportion of the foraging trip sitting on the water and had higher diving rate than males, suggesting higher foraging effort by females. In females, trip duration correlated with mass at departure, suggesting a flexible investment through control by body mass. The experimental study showed that handicapped females and female partners of handicapped males lost mass compared to control birds, whereas there was no difference for males. These results indicate that the larger female is the main provisioner of the chick in the pair, and regulates breeding effort in relation to its own body mass, whereas males have a fixed investment. The different breeding investment between the sexes is associated with contrasting foraging strategies, but no clear niche differentiation was observed. The larger size of the females may be advantageous for provisioning the chick with large quantities of energy and for flexible breeding effort, while the smaller male invests in territory defence and nest guarding, a crucial task when breeding at high densities. In masked boobies, division of labour appears to be maximal during chick rearing—the most energy-demanding period—and may be related to evolution of RSD.     

Sexual size dimorphism is not associated with the evolution of parental care in frogs

Sex differences in parental care are thought to arise from differential selection on the sexes. Sexual dimorphism, including sexual size dimorphism (SSD), is often used as a proxy for sexual selection on males. Some studies have found an association between male‐biased SSD (i.e., males larger than females) and the loss of paternal care. While the relationship between sexual selection on males and parental care evolution has been studied extensively, the relationship between female‐biased SSD (i.e., females larger than males) and the evolution of parental care has received very little attention. Thus, we have little knowledge of whether female‐biased SSD coevolves with parental care. In species displaying female‐biased SSD, we might expect dimorphism to be associated with the evolution of paternal care or perhaps the loss of maternal care. Here, drawing on data for 99 extant frog species, we use comparative methods to evaluate how parental care and female‐biased SSD have evolved over time. Generally, we find no significant correlation between the evolution of parental care and female‐biased SSD in frogs. This suggests that differential selection on body size between the sexes is unlikely to have driven the evolution of parental care in these clades and questions whether we should expect sexual dimorphism to exhibit a general relationship with the evolution of sex differences in parental care.     

Body mass dynamics during incubation and duration of parental care in Pacific Dunlins Calidris alpina pacifica: a test of the differential parental capacity hypothesis

Breeding is energetically expensive and individuals face a trade‐off between current and future breeding investment. Due to their production of large eggs, female birds are thought to have substantially higher initial energetic investments than males, which decrease the female's offspring rearing capacity. The differential parental capacity hypothesis argues that this large initial investment limits the ability of female shorebirds to provide extended parental care, which can ultimately lead to offspring desertion. This hypothesis predicts that (1) during early incubation females will be in poorer condition than males, (2) both sexes will lose condition during incubation, but the decline in females will be slower than the decline in males and (3) there will be a positive relationship between female condition and the duration of maternal brood care. These predictions were tested using data on body mass adjusted for body size (as a proxy for condition) and parental care from Pacific Dunlins Calidris alpina pacifica nesting on the Yukon Kuskokwim Delta, Alaska. None of the predictions received support: females were heavier than males in early incubation, the overall pattern during incubation was that males gained mass while female mass remained relatively constant, and there was no relationship between female mass and maternal brood care duration. These results suggest that the factors influencing parental care decisions are more complex than a parent simply caring until it is physiologically unable to do so.     

Directional changes in sexual size dimorphism in shorebirds, gulls and alcids

The Charadrii (shorebirds, gulls and alcids) are one of the most diverse avian groups from the point of view of sexual size dimorphism, exhibiting extremes in both male-biased and female-biased dimorphism, as well as monomorphism. In this study we use phylogenetic comparative analyses to investigate how size dimorphism has changed over evolutionary time, distinguishing between changes that have occurred in females and in males. Independent contrasts analyses show that both body mass and wing length have been more variable in males than in females. Directional analyses show that male-biased dimorphism has increased after inferred transitions towards more polygynous mating systems. There have been analogous increases in female-biased dimorphism after transitions towards more socially polyandrous mating systems. Changes in dimorphism in both directions are attributable to male body size changing more than female body size. We suggest that this might be because females are under stronger natural selection constraints related to fecundity. Taken together, our results suggest that the observed variation in dimorphism of Charadrii can be best explained by male body size responding more sensitively to variable sexual selection than female body size.     

Post-hatching parental care masks the effects of egg size on offspring fitness: a removal experiment on burying beetles

Parents can increase the fitness of their offspring by allocating nutrients to eggs and/or providing care for eggs and offspring. Although we have a good understanding of the adaptive significance of both egg size and parental care, remarkably little is known about the co-evolution of these two mechanisms for increasing offspring fitness. Here, we report a parental removal experiment on the burying beetle Nicrophorus vespilloides in which we test whether post-hatching parental care masks the effect of egg size on offspring fitness. As predicted, we found that the parent's presence or absence had a strong main effect on larval body mass, whereas there was no detectable effect of egg size. Furthermore, egg size had a strong and positive effect on offspring body mass in the parent's absence, whereas it had no effect on offspring body mass in the parent's presence. These results support the suggestion that the stronger effect of post-hatching parental care on offspring growth masks the weaker effect of egg size. We found no correlation between the number and size of eggs. However, there was a negative correlation between larval body mass and brood size in the parent's presence, but not in its absence. These findings suggest that the trade-off between number and size of offspring is shifted from the egg stage towards the end of the parental care period and that post-hatching parental care somehow moderates this trade-off.