The evolution of sex roles: The importance of ecology and social environment.

Males and females often have different roles in reproduction, although the origin of these differences has remained controversial. Explaining the enigmatic reversed sex roles where males sacrifice their mating potential and provide full parental care is a particularly long-standing challenge in evolutionary biology. While most studies focused on ecological factors as the drivers of sex roles, recent research highlights the significance of social factors such as the adult sex ratio. To disentangle these propositions, here, we investigate the additive and interactive effects of several ecological and social factors on sex role variation using shorebirds (sandpipers, plovers, and allies) as model organisms that provide the full spectrum of sex role variation including some of the best-known examples of sex-role reversal. Our results consistently show that social factors play a prominent role in driving sex roles. Importantly, we show that reversed sex roles are associated with both male-skewed adult sex ratios and high breeding densities. Furthermore, phylogenetic path analyses provide general support for sex ratios driving sex role variations rather than being a consequence of sex roles. Together, these important results open future research directions by showing that different mating opportunities of males and females play a major role in generating the evolutionary diversity of sex roles, mating system, and parental care.

Complexity of avian evolution revealed by family-level genomes.

Despite tremendous efforts in the past decades, relationships among main avian lineages remain heavily debated without a clear resolution. Discrepancies have been attributed to diversity of species sampled, phylogenetic method and the choice of genomic regions1-3. Here we address these issues by analysing the genomes of 363 bird species4 (218 taxonomic families, 92% of total). Using intergenic regions and coalescent methods, we present a well-supported tree but also a marked degree of discordance. The tree confirms that Neoaves experienced rapid radiation at or near the Cretaceous-Palaeogene boundary. Sufficient loci rather than extensive taxon sampling were more effective in resolving difficult nodes. Remaining recalcitrant nodes involve species that are a challenge to model due to either extreme DNA composition, variable substitution rates, incomplete lineage sorting or complex evolutionary events such as ancient hybridization. Assessment of the effects of different genomic partitions showed high heterogeneity across the genome. We discovered sharp increases in effective population size, substitution rates and relative brain size following the Cretaceous-Palaeogene extinction event, supporting the hypothesis that emerging ecological opportunities catalysed the diversification of modern birds. The resulting phylogenetic estimate offers fresh insights into the rapid radiation of modern birds and provides a taxon-rich backbone tree for future comparative studies.

Evolution of reproductive modes in sharks and rays.

The ecological and life history drivers of the diversification of reproductive modes in early vertebrates are not fully understood. Sharks, rays and chimaeras (group Chondrichthyes) have an unusually diverse variety of reproductive modes and are thus an ideal group to test the factors driving the evolution of reproductive complexity. Here, using 960 species representing all major Chondrichthyes taxa, we reconstruct the evolution of their reproduction modes and investigate the ecological and life history predictors of reproduction. We show that the ancestral Chondrichthyes state was egg-laying and find multiple independent transitions between egg-laying and live-bearing via an intermediate state of yolk-only live-bearing. Using phylogenetically informed analysis, we also show that live-bearing species have larger body size and larger offspring than egg-laying species. In addition, live-bearing species are distributed over shallow to intermediate depths, while egg-layers are typically found in deeper waters. This suggests that live-bearing is more closely associated with pelagic, rather than demersal habitats. Taken together, using a basal vertebrate group as a model, we demonstrat how reproductive mode co-evolves with environmental conditions and life-history traits.

Multiple paternity is related to adult sex ratio and sex determination system in reptiles.

The adult sex ratio (ASR, the proportion of males in the adult population) is an emerging predictor of reproductive behaviour, and recent studies in birds and humans suggest it is a major driver of social mating systems and parental care. ASR may also influence genetic mating systems. For instance male-skewed ASRs are expected to increase the frequency of multiple paternity (defined here as a clutch or litter sired by two or more males) due to higher rates of coercive copulations by males, and/or due to females exploiting the opportunity of copulation with multiple males to increase genetic diversity of their offspring. Here, we evaluate this hypothesis in reptiles that often exhibit high frequency of multiple paternity although its ecological and life-history predictors have remained controversial. Using a comprehensive dataset of 81 species representing all four non-avian reptile orders, we show that increased frequency of multiple paternity is predicted by more male-skewed ASR, and this relationship is robust to simultaneous effects of several life-history predictors. Additionally, we show that the frequency of multiple paternity varies with the sex determination system: species with female heterogamety (ZZ/ZW sex chromosomes) exhibit higher levels of multiple paternity than species with male heterogamety (XY/XX) or temperature-dependent sex determination. Thus, our across-species comparative study provides the first evidence that genetic mating system depends on ASR in reptiles. We call for further investigations to uncover the complex evolutionary associations between mating systems, sex determination systems and ASR.

Double-brooding and annual breeding success of great tits in urban and forest habitats.

Urban areas differ from natural habitats in several environmental features that influence the characteristics of animals living there. For example, birds often start breeding seasonally earlier and fledge fewer offspring per brood in cities than in natural habitats. However, longer breeding seasons in cities may increase the frequency of double-brooding in urban compared with nonurban populations, thus potentially increasing urban birds' annual reproductive output and resulting in lower habitat difference in reproductive success than estimated by studies focusing on first clutches only. In this study, we investigated 2 urban and 2 forests great tit Parus major populations from 2013 to 2019. We compared the probability of double-brooding and the total number of annually fledged chicks per female between urban and forest habitats, while controlling for the effects of potentially confounding variables. There was a trend for a higher probability of double-brooding in urban (44% of females) than in forest populations (36%), although this was not consistent between the 2 urban sites. Females produced significantly fewer fledglings annually in the cities than in the forest sites, and this difference was present both within single- and double-brooded females. Furthermore, double-brooded urban females produced a similar number of fledglings per season as single-brooded forest females. These results indicate that double-brooding increases the reproductive success of female great tits in both habitats, but urban females cannot effectively compensate in this way for their lower reproductive output per brood. However, other mechanisms like increased post-fledging survival can mitigate habitat differences in reproductive success.

Adult sex ratios: causes of variation and implications for animal and human societies.

Converging lines of inquiry from across the social and biological sciences target the adult sex ratio (ASR; the proportion of males in the adult population) as a fundamental population-level determinant of behavior. The ASR, which indicates the relative number of potential mates to competitors in a population, frames the selective arena for competition, mate choice, and social interactions. Here we review a growing literature, focusing on methodological developments that sharpen knowledge of the demographic variables underlying ASR variation, experiments that enhance understanding of the consequences of ASR imbalance across societies, and phylogenetic analyses that provide novel insights into social evolution. We additionally highlight areas where research advances are expected to make accelerating contributions across the social sciences, evolutionary biology, and biodiversity conservation.

The evolution of parental care in salamanders.

Complex parenting has been proposed to contribute to the evolutionary success of vertebrates. However, the evolutionary routes to complex parenting and the role of parenting in vertebrate diversity are still contentious. Although basal vertebrates provide clues to complex reproduction, these are often understudied. Using 181 species that represent all major lineages of an early vertebrate group, the salamanders and newts (Caudata, salamanders henceforth) here we show that fertilisation mode is tied to parental care: male-only care occurs in external fertilisers, whereas female-only care exclusively occurs in internal fertilisers. Importantly, internal fertilisation opens the way to terrestrial reproduction, because fertilised females are able to deposit their eggs on land, and with maternal care provision, the eggs could potentially develop outside the aquatic environment. Taken together, our results of a semi-aquatic early vertebrate group propose that the diversity and follow-up radiation of terrestrial vertebrates are inherently associated with a complex social behaviour, parenting.

Annual egg productivity predicts female-biased mortality in avian species.

Among avian species, the differential cost entailed by either sex in competition for mates has been regarded as the main evolutionary influence on sex differences in mortality rates. However, empirical evidence suggests that sex-biased adult mortality is mainly related to differential energy investment in gamete production, with a greater annual mass devoted to egg production leading to higher female mortality. We explicitly tested the generality of this pattern in a comparative framework. Annual egg production can be relatively large in some species (up to 200% of female body mass) and annual mortality is generally biased toward females. We showed that greater annual egg productivity resulted in higher mortality rates of females relative to males. Mating system was secondarily important, with species in which males were more involved in mating competition having more equal mortality rates between the sexes. However, both traits explained only a limited fraction of the interspecific variation in female-biased mortality. Other traits, such as sexual size dimorphism and parental care, had much weaker influences on female-biased mortality. Our results suggest that both annual mass devoted to gamete production by females and mating system contribute to the evolution of the fundamental life-history trade-off between reproduction and survival in avian taxa.

Evolution of Social Organization: Phylogenetic Analyses of Ecology and Sexual Selection in Weavers.

AbstractCrook published a landmark study on the social organization of weavers (or weaverbirds, family Ploceidae) that contributed to the emergence of sociobiology, behavioral ecology, and phylogenetic comparative methods. By comparing ecology, spatial distribution, and mating systems, Crook suggested that the spatial distribution of food resources and breeding habitats influence weaver aggregation during both the nonbreeding season (flocking vs. solitary foraging) and the breeding season (colonial vs. solitary breeding), and the latter in turn impacts mating systems and sexual selection. Although Crook's study stimulated much follow-up research, his conclusions have not been scrutinized using phylogenetically controlled analyses. We revisited Crook's hypotheses using modern phylogenetic comparative methods on an extended data set of 107 weaver species. We showed that both diet and habitat type are associated with spatial distribution and that the latter predicts mating system, consistent with Crook's propositions. The best-supported phylogenetic path model also supported Crook's arguments and uncovered a direct relationship between nonbreeding distribution and mating system. Taken together, our phylogenetically corrected analyses confirm Crook's conjectures on the roles of ecology in social organizations of weavers; however, our analyses also uncovered an association between nonbreeding distributions and mating systems, which was not envisaged by Crook.

Latitudinal gradients in avian colourfulness.

It has long been suggested that tropical species are generally more colourful than temperate species, but whether latitudinal gradients in organismal colourfulness exist remains controversial. Here we quantify global latitudinal trends in colourfulness (within-individual colour diversity) by collating and analysing a photographic dataset of whole-body plumage reflectance information for >4,500 species of passerine birds. We show that male and female birds of tropical passerine species are generally more colourful than their temperate counterparts, both on average and in the extreme. We also show that these geographic gradients can be explained in part by the effects of several latitude-related factors related to classic hypotheses for climatic and ecological determinants of organismal colourfulness. Taken together, our results reveal that species' colourfulness peaks in the tropics for passerine birds, confirming the existence of a long-suspected yet hitherto elusive trend in the distribution of global biodiversity.

Sex roles in birds: Phylogenetic analyses of the influence of climate, life histories and social environment.

Sex roles describe sex differences in courtship, mate competition, social pair-bonds and parental care. A key challenge is to identify associations among the components and the drivers of sex roles. Here, we investigate sex roles using data from over 1800 bird species. We found extensive variation and lability in proxies of sex roles, indicating remarkably independent evolution among sex role components. Climate and life history showed weak associations with sex roles. However, adult sex ratio is associated with sexual dimorphism, mating system and parental care, suggesting that social environment is central to explaining variation in sex roles among birds. Our results suggest that sex differences in reproductive behaviour are the result of diverse and idiosyncratic responses to selection. Further understanding of sex roles requires studies at the population level to test how local responses to ecology, life histories and mating opportunities drive processes that shape sex role variation among higher taxa.

Great tits feed their nestlings with more but smaller prey items and fewer caterpillars in cities than in forests.

Rapidly increasing urbanisation is one of the most significant anthropogenic environmental changes which can affect demographic traits of animal populations, for example resulting in reduced reproductive success. The food limitation hypothesis suggests that the shortage of high-quality nestling food in cities is a major factor responsible for the reduced reproductive performance in insectivorous birds. To study this explanation, we collected data on the parental provisioning behaviour of urban and forest great tits (Parus major) in three years that varied both in caterpillar availability (the main food of great tit nestlings) and in reproductive success of the birds. In all years, urban parents provisioned caterpillars in a smaller proportion to their nestlings, but the total amount of food per nestling (estimated by the volumes of all prey items) did not differ between habitats. In the two years with much lower reproductive success in urban than forest habitats, urban parents had higher provisioning rates, but provided more non-arthropod food and brought smaller prey items than forest parents. In the year with reduced habitat difference in reproductive success, urban parents were able to compensate for the scarcity of caterpillars by provisioning other arthropods rather than non-arthropod food, and by delivering larger preys than in the other years. Specifically, in this latter year, caterpillars provisioned by urban pairs were cc. twice as large as in the other two years, and were similar in size to caterpillars provisioned in the forest broods. These results show that although urban great tit parents can provide the same quantity of food per nestling as forest parents by reducing their brood size and increasing the per capita feeding rates for nestlings, they cannot compensate fully for the scarcity of high-quality preys (caterpillars) in poor years. In some years, however, favourable conditions for urban caterpillar development can greatly reduce food limitation in cities, allowing urban birds to achieve higher reproductive success. We suggest that urban green areas designed and managed in a way to facilitate conditions for phytophagous arthropods could improve habitat quality for urban birds.

Degree of anisogamy is unrelated to the intensity of sexual selection.

Males and females often display different behaviours and, in the context of reproduction, these behaviours are labelled sex roles. The Darwin-Bateman paradigm argues that the root of these differences is anisogamy (i.e., differences in size and/or function of gametes between the sexes) that leads to biased sexual selection, and sex differences in parental care and body size. This evolutionary cascade, however, is contentious since some of the underpinning assumptions have been questioned. Here we investigate the relationships between anisogamy, sexual size dimorphism, sex difference in parental care and intensity of sexual selection using phylogenetic comparative analyses of 64 species from a wide range of animal taxa. The results question the first step of the Darwin-Bateman paradigm, as the extent of anisogamy does not appear to predict the intensity of sexual selection. The only significant predictor of sexual selection is the relative inputs of males and females into the care of offspring. We propose that ecological factors, life-history and demography have more substantial impacts on contemporary sex roles than the differences of gametic investments between the sexes.

Contrasting effects of the COVID-19 lockdown on urban birds' reproductive success in two cities.

The ubiquitous activity of humans is a fundamental feature of urban environments affecting local wildlife in several ways. Testing the influence of human disturbance would ideally need experimental approach, however, in cities, this is challenging at relevant spatial and temporal scales. Thus, to better understand the ecological effects of human activity, we exploited the opportunity that the city-wide lockdowns due to the COVID-19 pandemic provided during the spring of 2020. We assessed changes in reproductive success of great tits (Parus major) at two urban habitats affected strikingly differently by the 'anthropause', and at an unaffected forest site. Our results do not support that urban great tits benefited from reduced human mobility during the lockdown. First, at one of our urban sites, the strongly (- 44%) reduced human disturbance in 2020 (compared to a long-term reference period) did not increase birds' reproductive output relative to the forest habitat where human disturbance was low in all years. Second, in the other urban habitat, recreational human activity considerably increased (+ 40%) during the lockdown and this was associated with strongly reduced nestling body size compared to the pre-COVID reference year. Analyses of other environmental factors (meteorological conditions, lockdown-induced changes in air pollution) suggest that these are not likely to explain our results. Our study supports that intensified human disturbance can have adverse fitness consequences in urban populations. It also highlights that a few months of 'anthropause' is not enough to counterweight the detrimental impacts of urbanization on local wildlife populations.

Evolution of large males is associated with female-skewed adult sex ratios in amniotes.

Body size often differs between the sexes (leading to sexual size dimorphism, SSD), as a consequence of differential responses by males and females to selection pressures. Adult sex ratio (ASR, the proportion of males in the adult population) should influence SSD because ASR relates to both the number of competitors and available mates, which shape the intensity of mating competition and thereby promotes SSD evolution. However, whether ASR correlates with SSD variation among species has not been yet tested across a broad range of taxa. Using phylogenetic comparative analyses of 462 amniotes (i.e., reptiles, birds, and mammals), we fill this knowledge gap by showing that male bias in SSD increases with increasingly female-skewed ASRs in both mammals and birds. This relationship is not explained by the higher mortality of the larger sex because SSD is not associated with sex differences in either juvenile or adult mortality. Phylogenetic path analysis indicates that higher mortality in one sex leads to skewed ASR, which in turn may generate selection for SSD biased toward the rare sex. Taken together, our findings provide evidence that skewed ASRs in amniote populations can result in the rarer sex evolving large size to capitalize on enhanced mating opportunities.

Social organization in ungulates: Revisiting Jarman's hypotheses.

Ungulates (antelopes, deer and relatives) have some of the most diverse social systems among mammals. To understand the evolution of ungulate social organization, Jarman (1974) proposed an ecological scenario of how distribution of resources, habitat and feeding style may have influenced social organization. Although Jarman's scenario makes intuitive sense and remains a textbook example of social evolution, it has not been scrutinized using modern phylogenetic comparative methods. Here we use 230 ungulate species from ten families to test Jarman's hypotheses using phylogenetic analyses. Consistent with Jarman's proposition, both habitat and feeding style predict group size, since grazing ungulates typically live in open habitats and form large herds. Group size, in turn, has a knock-on effect on mating systems and sexual size dimorphism, since ungulates that live in large herds exhibit polygamy and extensive sexual size dimorphism. Phylogenetic confirmatory path analyses suggest that evolutionary changes in habitat type, feeding style and body size directly (or indirectly) induce shifts in social organization. Taken together, these phylogenetic comparative analyses confirm Jarman's conjectures, although they also uncover novel relationships between ecology and social organization. Further studies are needed to explore the relevance of Jarman (1974) scenario for mammals beyond ungulates.

Are evolutionary transitions in sexual size dimorphism related to sex determination in reptiles?

Sex determination systems are highly variable in vertebrates, although neither the causes nor the implications of this diversity are fully understood. Theory suggests that sex determination is expected to relate to sexual size dimorphism, because environmental sex determination promotes sex-specific developmental bias in embryonic growth rates. Furthermore, selection for larger size in one sex or the other has been proposed to drive the evolution of different genetic sex determination systems. Here, we investigate whether sex determination systems relate to adult sexual size dimorphism, using 250 species of reptiles (Squamata, Testudines and Crocodylia) representing 26 families. Using phylogenetically informed analyses, we find that sexual size dimorphism is associated with sex determination: species with TSDIa sex determination (i.e. in which the proportion of female offspring increases with incubation temperature) have more female-biased size dimorphism than species with TSDII (i.e. species in which males are produced at mid temperatures). We also found a trend that species with TSD ancestors had more male-biased size dimorphism in XY sex chromosome systems than in ZW sex chromosome systems. Taken together, our results support the prediction that sexual size dimorphism is linked to sex-dependent developmental variations caused by environmental factors and also by sex chromosomes. Since the extent of size dimorphism is related to various behavioural, ecological and life-history differences between sexes, our results imply profound impacts of sex determination systems for vertebrate diversity.

Mortality cost of sex-specific parasitism in wild bird populations.

Sex-specific mortality is frequent in animals although the causes of different male versus female mortalities remain poorly understood. Parasitism is ubiquitous in nature with widespread detrimental effects to hosts, making parasitism a likely cause of sex-specific mortalities. Using sex-specific blood and gastrointestinal parasite prevalence from 96 and 54 avian host species, respectively, we test the implications of parasites for annual mortality in wild bird populations using phylogenetic comparative methods. First, we show that parasite prevalence is not different between adult males and females, although Nematodes showed a statistically significant but small male-biased parasite prevalence. Second, we found no correlation between sex-biased host mortalities and sex-biased parasite prevalence. These results were consistent in both blood and gastrointestinal parasites. Taken together, our results show little evidence for sex-dependent parasite prevalence in adults in wild bird populations, and suggest that parasite prevalence is an unlikely predictor of sex difference in adult mortalities, not withstanding sampling limitations. We propose that to understand causes of sex-biased mortalities, more complex analyses are needed that incorporate various ecological and life history components of animals life that may include sex differences in exposure to predators, immune capacity and cost of reproduction.