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.     

Brain size evolution in pipefishes and seahorses: the role of feeding ecology,life history and sexual selection

Brain size varies greatly at all taxonomic levels. Feeding ecology, life history and sexual selection have been proposed as key components in generating contemporary diversity in brain size across vertebrates. Analyses of brain size evolution have, however, been limited to lineages where males predominantly compete for mating and females choose mates. Here, we present the first original data set of brain sizes in pipefishes and seahorses (Syngnathidae) a group in which intense female mating competition occurs in many species. After controlling for the effect of shared ancestry and overall body size, brain size was positively correlated with relative snout length. Moreover, we found that females, on average, had 4.3% heavier brains than males and that polyandrous species demonstrated more pronounced (11.7%) female‐biased brain size dimorphism. Our results suggest that adaptations for feeding on mobile prey items and sexual selection in females are important factors in brain size evolution of pipefishes and seahorses. Most importantly, our study supports the idea that sexual selection plays a major role in brain size evolution, regardless of on which sex sexual selection acts stronger.     

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.     

The Role of Courtship Behavior and Size in Mate Preference in the Sex‐Role‐Reversed Gulf Pipefish,Syngnathus scovelli

In sex‐role‐reversed species, sexual selection acts more strongly on females than on males, a situation that can result in the evolution of secondary sexual traits in females and strong mating preferences in males. While some research exploring mating preferences in sex‐role‐reversed species has been conducted, overall, this topic remains relatively unexplored. The Gulf pipefish, Syngnathus scovelli, is a highly polyandrous pipefish species. Sexual selection is significantly stronger in females than in males, which has led to the evolution of both morphological and behavioral female secondary sexual traits. However, because males gestate the offspring in specialized pouches and make a substantial investment in embryos during development, females may also benefit from being choosy. The goal of this study was to examine both male and female mating preferences in this species. We found that male mating preference was significantly associated with female courtship behavior. Larger females were also able to maintain these behaviors for longer intervals than smaller females. No evidence of female mating preference in regard to male size was observed but the data suggest that male behaviors may be providing positive reinforcement to courting females. This research provides further insight into how mate preferences vary among sex‐role‐reversed species.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

The evolution of egg size in socially polyandrous shorebirds

In classical and multi-clutch polyandry, females lay multiple clutches during a breeding season for more than one mate. The production of multiple clutches may be energetically demanding. We used comparative analyses to investigate three possible ways of reducing such egg-laying costs in polyandrous shorebirds: (1) reduction in egg size, (2) reduction in clutch size, and (3) evolutionary increase in female size. Paired comparisons of polyandrous and non-polyandrous taxa showed that females of polyandrous shorebirds lay smaller eggs than females of closely related monogamous and polygynous species. Directional analyses corroborated this result by indicating a significant decrease in egg size after phylogenetically independent origins of polyandry. The comparative analyses uniformly rejected the two alternatives, i.e. neither clutch size nor female size is related to social mating pattern. We also tested and rejected three alternative explanations for reduced egg size in polyandrous taxa. First, we found no evidence that polyandrous females have evolved smaller egg sizes in response to selection to match smaller size of males, which provide the parental care in these species. Second, reduction in egg size was not related to longer breeding seasons (and hence more opportunity for re-nesting). Third, reduced egg sizes were also not related to rates of clutch predation (another potential correlate of multiple clutch production). Our results are thus consistent with the hypothesis that selection for reducing laying costs explains small egg size in socially polyandrous shorebirds.     

Sexual behaviour and evolution of sexual dimorphism in body size in Jaera (Isopoda Asellota)

Individuals of the genus Jaera do not mate at random. In the species from the Mediterranean group, J. italica and. J. nordmanni, large males and medium sized females are at an advantage and their sizes are positively assorted. These effects are attributable to sexual competition between males. In the Ponlo-caspian species J. istri, no advantage of large males exists, but sexual selection could be the cause for a long passive phase prior to copulation and for normalizing selection upon female size at pairing. In the Atlantic species, J. albifrons, no selection can be ascertained.
Differential mating success in males appears as one of the causes of the evolution of sexual dimorphism in body size, which makes males larger, of equal size, or smaller than females according to the species. The reason for this reversal in dimorphism seems to differ in the two sexes. Sexual selection provides an explanation for the evolution of male size, while the interspecific changes in female length are more likely due to ecological factors.     

Sexual selection and senescence: do seed beetle males (Acanthoscelides obtectus,Bruchidae, Coleoptera) shape the longevity of their mates?

Although the reasons why organisms age and die are generally well understood, it has recently been suggested that an optimal life span has evolved not only as the result of trade‐offs between reproductive performances early and late in life, but also that a balance between the costs and benefits of the number of mating has also played an important role in the evolution of ageing in both sexes. By using four seed beetle (Acanthoscelides obtectus) lines selected for different life history traits, but which have also inadvertently created monoandrous and polyandrous conditions, we showed that males evolved to affect the mortality patterns of females in a way consistent to the postmating sexual selection generated by sexually antagonistic co‐evolution theory. Monoandrous males, irrespectively of body weight and other life history traits specific to their lines, evolved to increase the longevity of control females kept under starvation and suppressed fecundity, compared with males that originated in the lines with effectively polyandrous conditions. When females were allowed to lay eggs, the effects of males from different lines and mating type history on the senescence of females were substantially weaker. We found that males in the line that was evolved to decelerate senescence and polyandrous conditions stimulate the earlier onset of females’ oviposition, relative to males stemmed from the line with accelerated senescence and monoandrous conditions. This fact may explain the absence of difference in the mean longevities between the control females mated to these males and highlight the importance of sexual selection in the evolution of ageing.     

Evolution of Classical Polyandry: Three Steps to Female Emancipation

Abstract In classical polyandry, sex roles are reversed and a female reproduces with several males, each of whom raises his offspring with little or no help from her. This mating system occurs in some fishes and birds, and it is of great interest in relation to parental investment, sex role and sexual selection theory. The evolution of classical polyandry, however, is debated and not well understood. It is here suggested to generally take place in three main steps. (1) First evolves male care for eggs, for reasons that differ between fishes and birds. (2) Second, a female becomes able to lay more eggs than a male can accommodate. This can happen, for example, by evolution of male pregnancy or smaller body size, or by female production of more or larger eggs, made possible by larger female body size or more food. Polyandry in several taxa is associated with shift to a habitat rich in food during the breeding season, to novel specialised foraging methods, or to both. A favourable food situation may be crucial for evolution of classical polyandry. (3) In step three, females compete to lay two or more clutches in sequence for different males. Successful polyandrous females obtain more offspring, spreading traits that enhance success in competition over males. Step three may be most likely in species with small body size, for reasons of reproductive constraints and seasonality. Evolution of classical polyandry appears to have followed these steps in shorebirds, coucals and pipefishes, but the reasons why certain species differ from their close phylogenetic relatives in being polyandrous are far from clear. Behavioural and ecological studies of additional species, and detailed phylogenies of taxa with diverse mating systems including polyandry, are needed for testing these ideas.     

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.     

Female‐biased size dimorphism in a diapausing caddisfly,Mesophylax aspersus: effect of fecundity and natural and sexual selection

1. The effect of mating success, female fecundity and survival probability associated with intra‐sex variation in body size was studied in Mesophylax aspersus, a caddisfly species with female‐biased sexual size dimorphism, which inhabits temporary streams and aestivates in caves. Adults of this species do not feed and females have to mature eggs during aestivation. 2. Thus, females of larger size should have a fitness advantage because they can harbour more energy reserves that could influence fecundity and probability of survival until reproduction. In contrast, males of smaller size might have competitive advantages over others in mating success. 3. These hypotheses were tested by comparing the sex ratio and body size of individuals captured before and after the aestivation period. The associations between body size and female fecundity, and between mating success and body size of males, were explored under laboratory conditions. 4. During the aestivation period, the sex ratio changed from 1 : 1 to male biased (4 : 1), and a directional selection on body size was detected for females but not for males. Moreover, larger clutches were laid by females of larger size. Finally, differences in mating success between small and large males were not detected. These results suggest that natural selection (i.e. the differential mortality of females associated with body size) together with possible fecundity advantages, are important factors responsible of the sexual size dimorphism of M. aspersus. 5. These results highlight the importance of taking into account mechanisms other than those traditionally used to explain sexual dimorphism. Natural selection acting on sources of variation, such as survival, may be as important as fecundity and sexual selection in driving the evolution of sexual size dimorphism.     

Front Cover

In most animals, competition for mating opportunities is higher among males, whereas females are more likely to provide parental care. In few species, though, these "conventional" sex roles are reversed such that females compete more strongly for matings and males provide most or all parental care. This "reversal" in sex roles is often combined with classical polyandry—a mating system in which a female forms a harem with several males. Here, we review the major hypotheses relating such role reversals to evolutionary and behavioural traits (anisogamy, phylogenetic history, sexy males, parental care, genetic paternity, trade‐off between mating and parenting, adult sex ratio) and to ecological factors (food supply, offspring predation). We evaluate each hypothesis in relation to coucals (Centropodinae), a group of nesting cuckoos of great interest for mating system and parental care theory. The black coucal (Centropus grillii) is the only known bird combining classical polyandry with altricial development of young, a costly trait with regard to parental care. Our long‐term study offers a unique possibility to compare the strongly polyandrous black coucal with a monogamous close relative breeding in the same area and habitat, the white‐browed coucal (C. superciliosus). We show that the evolution of sex roles in coucals and other animals has many different facets. Whereas phylogenetic constraints are important, confidence in genetic paternity is not. In combination with facilitating ecological conditions, adult sex ratios are key to understanding sex roles in coucals, shorebirds, and most likely also other animals. We plead for more studies including experimental tests to understand how biased adult sex ratios emerge and whether they drive sexual selection or vice versa. How do sex ratios and sexual selection interact and feedback on each other? Answers to these questions will be fundamental for understanding the evolution of sex roles in mating and parenting in coucals and other species.     

Sexual selection and senescence: male size-dimorphic ungulates evolved relatively smaller molars than females

As a general rule, males of sexually dimorphic ungulate species have evolved larger body size than females but shorter reproductive life spans as elements of their strategy for intrasexual competition for mating opportunities. Evolutionary theories of senescence predict that the durability of somatic structures should relate to the length of reproductive life span. This prediction has recently been tested for red deer (Cervus elaphus): molariform teeth of males are smaller and less durable than those of females, which corresponds with sex differences in reproductive life span. However, general evidence that male teeth are smaller than expected by allometric rules as a consequence of sexual selection for increasing male body mass requires an interspecific comparison between dimorphic and nondimorphic ungulates. Here we investigate the relationship between cheek-teeth size (occlusal surface area; OSA) and body mass in 123 species of extant ungulates. We found lower slopes for dimorphic species compared with nondimorphic ones and smaller OSA, relative to body mass, in males of dimorphic species compared with females of dimorphic species. Rates of evolution of OSA relative to rates of evolution of body mass were greater in females than in males and also greater in nondimorphic than in dimorphic species. Our results are consistent with the hypothesis that sexual selection in polygynous male ungulates favors body size more than tooth size, with possible consequences in male senescence via early depletion of male teeth compared to females.     

Unpredictable environments,nuptial gifts and the evolution of sexual size dimorphism in insects: an experiment

Many insects have a mating system where males transfer nutrients to females at mating, which are often referred to as ''nuptial gifts''. Among butterflies, some of the characteristic features of these species are polyandry (females mate multiple times), and relatively large male ejaculates. When males produce part of the resources used for offspring, the value of body size might then increase for males and decrease for females. The male/female size ratio is also observed to increase when the degree of polyandry and gift size increase. Butterfly species where gift-giving occurs are generally more variable in body size, suggesting that food quality/quantity fluctuates during juvenile stages. This will cause some males to have much to provide and some females to be in great need, and could be conducive to the evolution of a gift-giving mating system. In such a system, growing male and female juveniles should react differently to food shortage. Females should react by maturing at a smaller size since their own lack of reproductive resources can partly be compensated for by male contributions. Males have to pay the full cost of decreased reproduction if they mature at a small size, making it more important for males to keep on growing, even when growth is costly. An earlier experiment with the polyandrous and gift-giving butterfly, Pieris napi, supported this prediction. The pattern is expected to be absent or reversed for species with small nuptial gifts, where females do not benefit from mating repeatedly, and will thus be dependent on acquiring resources for reproduction on their own. To test this prediction, we report here on an experiment with the speckled wood butterfly, Pararge aegeria. We find that growth response correlates with mating system in the two above species, and we conclude that differences in environmental conditions between species may act as an important factor in the evolution of the mating system and sexual size dimorphism.     

Mating systems and sexual selection in male-pregnant pipefishes and seahorses: insights from microsatellite-based studies of maternity

In pipefishes and seahorses (family Syngnathidae), the males provide all postzygotic care of offspring by brooding embryos on their ventral surfaces. In some species, this phenomenon of male "pregnancy" results in a reversal of the usual direction of sexual selection, such that females compete more than males for access to mates, and secondary sexual characteristics evolve in females. Thus the syngnathids can provide critical tests of theories related to the evolution of sex differences and sexual selection. Microsatellite-based studies of the genetic mating systems of several species of pipefishes and seahorses have provided insights into important aspects of the natural history and evolution of these fishes. First, males of species with completely enclosed pouches have complete confidence of paternity, as might be predicted from parental investment theory for species in which males invest so heavily in offspring. Second, a wide range of genetic mating systems have been documented in nature, including genetic monogamy in a seahorse, polygynandry in two species of pipefish, and polyandry in a third pipefish species. The genetic mating systems appear to be causally related to the intensity of sexual selection, with secondary sex characters evolving most often in females of the more polyandrous species. Third, genetic studies of captive-breeding pipefish suggest that the sexual selection gradient (or Bateman gradient) may be a substantially better method for characterizing the mating system than previously available techniques. Finally, these genetic studies of syngnathid mating systems have led to some general insights into the occurrence of clustered mutations at microsatellite loci, the utility of linked loci in studies of parentage, and the use of parentage data for direct estimation of adult population size.     

Sexual Selection in the Water Spider: Female Choice and Male–Male Competition

The water spider Argyroneta aquatica is the only spider spending its whole life under water, and one of the few spider species in which males are larger than females. Previous studies indicated that males can cannibalize females, which is uncommon among spiders. Here we aimed to further test for a potential influence of sexual selection on male body size. We examined the importance of female choice by testing whether females prefer the larger of two simultaneously presented males as mating partners. Further, we examined the influence of male–male competition by comparing the fighting behaviour between large and small males when alone or when together with a female, and we determined the outcome of fights. We found that females approach and choose large males as mating partners, despite the risk of male cannibalism. Additionally, males intensively compete for females, and large males clearly win against smaller ones. Hence sexual selection seems to be important for the evolution of the peculiar sexual size dimorphism of water spiders, as large size is beneficial for males in both the intra‐ and intersexual context. Previous studies have suggested an important role of natural selection in the sex‐specific body size of water spiders, but natural and sexual selection mechanisms apparently work in the same direction, favouring large male size.     

Linking intra‐ and interspecific assortative mating: Consequences for asymmetric sexual isolation

Assortative mating is of interest because of its role in speciation and the maintenance of species boundaries. However, we know little about how within‐species assortment is related to interspecific sexual isolation. Most previous studies of assortative mating have focused on a single trait in males and females, rather than utilizing multivariate trait information. Here, we investigate how intraspecific assortative mating relates to sexual isolation in two sympatric and congeneric damselfly species (genus Calopteryx). We connect intraspecific assortment to interspecific sexual isolation by combining field observations, mate preference experiments, and enforced copulation experiments. Using canonical correlation analysis, we demonstrate multivariate intraspecific assortment for body size and body shape. Males of the smaller species mate more frequently with heterospecific females than males of the larger species, which showed less attraction to small heterospecific females. Field experiments suggest that sexual isolation asymmetry is caused by male preferences for large heterospecific females, rather than by mechanical isolation due to interspecific size differences or female preferences for large males. Male preferences for large females and male–male competition for high quality females can therefore counteract sexual isolation. This sexual isolation asymmetry indicates that sexual selection currently opposes a species boundary.     

On the role of sexual selection in ecological divergence: a test of body‐size assortative mating in the eastern newt Notophthalmus viridescens

Speciation processes initiated by divergent selection often fail to complete; yet, how sexual selection is involved in the progress of ecological speciation is rarely understood. Intraspecific body‐size variation affects mate preference and male–male competition, which can consequently lead to assortative mating based on body size. In the present study, we tested the importance of body size difference in the potential of assortative mating between the two eastern newt subspecies, larger Notophthalmus viridescens viridescens and smaller Notophthalmus viridescens dorsalis. Through differential expression of life‐cycle polyphenism, these two subspecies are adapted to contrasting environments, which has likely led to the subspecific body‐size difference. We found that males of both subspecies preferred larger females of N. v. viridescens as mates presumably because of the fecundity advantage of larger females. On the other hand, no evidence of female choice was found. Larger males of N. v. viridescens exhibited greater competitive ability and gained primary access to larger females of their own kind. However, smaller males were able to overcome their inferior competitive ability by interfering with larger males' spermatophore transfer and sneakily mating with larger females. Thus, the subspecific body‐size difference importantly affected sexual selection processes, resulting in nonrandom but not completely assortative mating patterns between the larger and smaller subspecies. Although life‐cycle polyphenism facilitates the intraspecific ecological divergence within N. v. viridescens sexual selection processes, namely smaller males' mate preference for larger females and sexual interference during spermatophore transfer, may be halting completion of the ecological speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 884–897.     

Mating system and brain size in bats

The contribution of sexual selection to brain evolution has been little investigated. Through comparative analyses of bats, we show that multiple mating by males, in the absence of multiple mating by females, has no evolutionary impact on relative brain dimension. In contrast, bat species with promiscuous females have relatively smaller brains than do species with females exhibiting mate fidelity. This pattern may be a consequence of the demonstrated negative evolutionary relationship between investment in testes and investment in brains, both metabolically expensive tissues. These results have implications for understanding the correlated evolution of brains, behaviour and extravagant sexually selected traits.     

Post-copulatory sexual selection and female fitness in Scathophaga stercoraria

Whether sexual selection increases or decreases female fitness is determined by the occurrence and relative importance of sexual-conflict processes and the ability of females to choose high-quality males. Experimentally enforced polyandry and monogamy have previously been shown to cause rapid evolution in the yellow dung fly Scathophaga stercoraria. Flies from polyandrous lines invested more in reproductive tissue, and this investment influenced paternity in sperm competition, but came at a cost to immune function. While some fitness consequences of enforced polyandry or monogamy have been examined when flies mate multiply, the consequences for female fitness when singly copulated remain unexplored. Under a good-genes scenario females from polyandrous lines should be of higher general quality and should outperform females from monogamous lines even with a single copulation. Under sexual conflict, costly adaptations will afford no advantages when females are allowed to mate only once. We investigate the lifetime reproductive success and longevity of females evolving under enforced monogamy or polyandry when mating once with males from these selection regimes. Females from polyandrous lines were found to have lower fitness than their monogamous counterparts when mating once. They died earlier and produced significantly fewer eggs and offspring. These results suggest that sexual conflict probably drove evolution under enforced polyandry as female fitness did not increase overall as expected with purely good-genes effects.