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.

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.

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.

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.

Sex differences in adult lifespan and aging rates of mortality across wild mammals.

In human populations, women consistently outlive men, which suggests profound biological foundations for sex differences in survival. Quantifying whether such sex differences are also pervasive in wild mammals is a crucial challenge in both evolutionary biology and biogerontology. Here, we compile demographic data from 134 mammal populations, encompassing 101 species, to show that the female's median lifespan is on average 18.6% longer than that of conspecific males, whereas in humans the female advantage is on average 7.8%. On the contrary, we do not find any consistent sex differences in aging rates. In addition, sex differences in median adult lifespan and aging rates are both highly variable across species. Our analyses suggest that the magnitude of sex differences in mammalian mortality patterns is likely shaped by local environmental conditions in interaction with the sex-specific costs of sexual selection.

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.

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.

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.

The genetic sex-determination system predicts adult sex ratios in tetrapods.

The adult sex ratio (ASR) has critical effects on behaviour, ecology and population dynamics, but the causes of variation in ASRs are unclear. Here we assess whether the type of genetic sex determination influences the ASR using data from 344 species in 117 families of tetrapods. We show that taxa with female heterogamety have a significantly more male-biased ASR (proportion of males: 0.55 ± 0.01 (mean ± s.e.m.)) than taxa with male heterogamety (0.43 ± 0.01). The genetic sex-determination system explains 24% of interspecific variation in ASRs in amphibians and 36% in reptiles. We consider several genetic factors that could contribute to this pattern, including meiotic drive and sex-linked deleterious mutations, but further work is needed to quantify their effects. Regardless of the mechanism, the effects of the genetic sex-determination system on the adult sex ratio are likely to have profound effects on the demography and social behaviour of tetrapods.

Food availability limits avian reproduction in the city: An experimental study on great tits Parus major.

The altered ecological and environmental conditions in towns and cities strongly affect demographic traits of urban animal populations, for example avian reproductive success is often reduced. Previous work suggests that this is partly driven by low insect availability during the breeding season, but robust experimental evidence that supports this food limitation hypothesis is not yet available. We tested core predictions of the food limitation hypothesis using a controlled experiment that provided supplementary insect food (nutritionally enhanced mealworms supplied daily to meet 40%-50% of each supplemented brood's food requirements) to great tit nestlings in urban and forest habitats. We measured parental provisioning rates and estimated the amount of supplementary food consumed by control and experimental nestlings, and assessed their body size and survival rates. Provisioning rates were similar across habitats and control and supplemented broods, but supplemented (and not control) broods consumed large quantities of supplementary food. As predicted by the food limitation hypothesis we found that nestlings in (a) urban control broods had smaller body size and nestling survival rates than those in forest control broods; (b) forest supplemented and control broods had similar body size and survival rates; (c) urban supplemented nestlings had larger body size and survival rates than those in urban control broods; and crucially (d) urban supplemented broods had similar body size and survival rates to nestlings in forest control broods. Our results provide rare experimental support for the strong negative effects of food limitation during the nestling rearing period on urban birds' breeding success. Furthermore, the fact that supplementary food almost completely eliminated habitat differences in survival rate and nestling body size suggest that urban stressors other than food shortage contributed relatively little to the reduced avian breeding success. Finally, given the impacts of the amount of supplementary food that we provided and taking clutch size differences into account, our results suggest that urban insect populations in our study system would need to be increased by a factor of at least 2.5 for urban and forest great tits to have similar reproductive success.

Scavenging behaviour and size-dependent carcass consumption of the black bullhead (Ameiurus melas).

This study examined the size-dependent scavenging behaviour of black bullheads Ameiurus melas under laboratory conditions, using common bleak Alburnus alburnus and pumpkinseed Lepomis gibbosus carcasses. Video camera observations showed that the activity of A. melas was higher at night, but substantial daytime activity was also recorded. Larger A. melas were more active than their smaller conspecifics, especially at night. All size classes exhibited a well-defined sequence of consuming different parts of the carcasses independent of size, but larger individuals tended to consume carcasses more efficiently. Carcasses of the softer-bodied A. alburnus were consumed more readily than those of the bonier L. gibbosus, independent of size. This scavenging behaviour of A. melas might facilitate the invasion success of the species.

Sex ratios and bimaturism differ between temperature-dependent and genetic sex-determination systems in reptiles.

BACKGROUND: Sex-determining systems may profoundly influence the ecology, behaviour and demography of animals, yet these relationships are poorly understood. Here we investigate whether species with temperature-dependent (TSD) and genetic sex determination (GSD) differ in key demographic traits, using data from 181 species representing all major phylogenetic lineages of extant reptiles. RESULTS: We show that species with TSD exhibit significantly higher within-species variance in sex ratios than GSD species in three major life stages: birth or hatching, juvenility and adulthood. In contrast, sex differences in adult mortality rates do not differ between GSD and TSD species. However, TSD species exhibit significantly greater sex differences in maturation ages than GSD species. CONCLUSION: These results support the recent theoretical model that evolution of TSD is facilitated by sex-specific fitness benefits of developmental temperatures due to bimaturism. Our findings suggest that different sex-determination systems are associated with different demographic characteristics that may influence population viability and social evolution.

Parental care and the evolution of terrestriality in frogs.

Frogs and toads (Anura) exhibit some of the most diverse parental strategies in vertebrates. Identifying the evolutionary origins of parenting is fundamental to understanding the relationships between sexual selection, social evolution and parental care systems of contemporary Anura. Moreover, parenting has been hypothesized to allow the invasion of terrestrial habitats by the ancestors of terrestrial vertebrates. Using comprehensive phylogenetic analyses of frogs and toads based on data from over 1000 species that represent 46 out of 55 Anura families, we test whether parental care is associated with terrestrial reproduction and several life-history traits. Here, we show that both the duration of care and offspring protection by males and females have coevolved with terrestrial reproduction. Sexual size dimorphism is also related to care, because the large male size relative to female size is associated with increased paternal care. Furthermore, increased egg size and reduced clutch volume are associated with increased care in bivariate but not in multivariate analyses, suggesting that the relationships between care, egg size and clutch volume are mediated by terrestrial reproduction. Taken together, our results suggest that parenting by males and females has coevolved, and complex parenting traits have evolved several times independently in Anura in response to breeding in terrestrial environments.

Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird.

Urbanization can have marked effects on plant and animal populations' phenology, population size, predator-prey, interactions and reproductive success. These aspects are rarely studied simultaneously in a single system, and some are rarely investigated, e.g., how insect phenology responds to urban development. Here, we study a tri-trophic system of trees, phytophagous insects (caterpillars), and insectivorous birds (Great Tits) to assess how urbanization influences (1) the phenology of each component of this system, (2) insect abundance, and (3) avian reproductive success. We use data from two urban and two forest sites in Hungary, central Europe, collected over four consecutive years. Despite a trend of earlier leaf emergence in urban sites, there is no evidence for an earlier peak in caterpillar abundance. Thus, contrary to the frequently stated prediction in the literature, the earlier breeding of urban bird populations is not associated with an earlier peak in caterpillar availability. Despite this the seasonal dynamics of caterpillar biomass exhibited striking differences between habitat types with a single clear peak in forests, and several much smaller peaks in urban sites. Caterpillar biomass was higher in forests than urban areas across the entire sampling period, and between 8.5 and 24 times higher during the first brood's chick-rearing period. This higher biomass was not associated with taller trees in forest sites, or with tree species identity, and occurred despite most of our focal trees being native to the study area. Urban Great Tits laid smaller clutches, experienced more frequent nestling mortality from starvation, reared fewer offspring to fledging age, and their fledglings had lower body mass. Our study strongly indicates that food limitation is responsible for lower avian reproductive success in cities, which is driven by reduced availability of the preferred nestling diet, i.e., caterpillars, rather than phenological shifts in the timing of peak food availability.

The evolution of parental cooperation in birds.

Parental care is one of the most variable social behaviors and it is an excellent model system to understand cooperation between unrelated individuals. Three major hypotheses have been proposed to explain the extent of parental cooperation: sexual selection, social environment, and environmental harshness. Using the most comprehensive dataset on parental care that includes 659 bird species from 113 families covering both uniparental and biparental taxa, we show that the degree of parental cooperation is associated with both sexual selection and social environment. Consistent with recent theoretical models parental cooperation decreases with the intensity of sexual selection and with skewed adult sex ratios. These effects are additive and robust to the influence of life-history variables. However, parental cooperation is unrelated to environmental factors (measured at the scale of whole species ranges) as indicated by a lack of consistent relationship with ambient temperature, rainfall or their fluctuations within and between years. These results highlight the significance of social effects for parental cooperation and suggest that several parental strategies may coexist in a given set of ambient environment.

Problem-solving performance and reproductive success of great tits in urban and forest habitats.

Success in problem solving, a form of innovativeness, can help animals exploit their environments, and recent research suggests that it may correlate with reproductive success. Innovativeness has been proposed to be especially beneficial in urbanized habitats, as suggested by superior problem-solving performance of urban individuals in some species. If there is stronger selection for innovativeness in cities than in natural habitats, we expect problem-solving performance to have a greater positive effect on fitness in more urbanized habitats. We tested this idea in great tits (Parus major) breeding at two urban sites and two forests by measuring their problem-solving performance in an obstacle-removal task and a food-acquisition task. Urban pairs were significantly faster problem-solvers in both tasks. Solving speed in the obstacle-removal task was positively correlated with hatching success and the number of fledglings, whereas performance in the food-acquisition task did not correlate with reproductive success. These relationships did not differ between urban and forest habitats. Neophobia, sensitivity to human disturbance, and risk taking in the presence of a predator did not explain the relationships of problem-solving performance either with habitat type or with reproductive success. Our results suggest that the benefit of innovativeness in terms of reproductive success is similar in urban and natural habitats, implying that problem-solving skills may be enhanced in urban populations by some other benefits (e.g. increased survival) or reduced costs (e.g. more opportunities to gain practice with challenging tasks).

Does urbanization facilitate individual recognition of humans by house sparrows?

Wild animals living in proximity to humans may benefit from recognizing people individually and adjusting their behaviour to the potential risk or gain expected from each person. Although several urban-dwelling species exhibit such skills, it is unclear whether this is due to pre-existing advanced cognitive abilities of taxa predisposed for city life or arises specifically in urban populations either by selection or through ontogenetic changes facilitated by exposure to humans. To test these alternatives, we studied populations of house sparrows (Passer domesticus) along the urbanization gradient. We manipulated the birds' experience (hostile or not) associated with humans with different faces (masks) and measured their behavioural responses to the proximity of each person. Contrary to our expectations, we found that while rural birds showed less fear of the non-hostile than of the hostile or an unfamiliar person, urban birds made no distinction. These results indicate that house sparrows are less able to recognize individual humans or less willing to behaviourally respond to them in more urbanized habitats with high human population density. We propose several mechanisms that may explain this difference, including reduced pay-off of discrimination due to a low chance of repeated interactions with city people, or a higher likelihood that city people will ignore them.

Social role specialization promotes cooperation between parents.

Biparental care of offspring is a widespread social behavior, and various ecological, life-history, and demographic factors have been proposed to explain its evolution and maintenance. Raising offspring generally requires several types of care (e.g., feeding, brooding, and defense), and males and females often specialize in providing different types of care. However, theoretical models of care often assume that care is a single variable and hence that a unit of care by the mother is interchangeable with a unit of care by the father. We hypothesize that the ability of one parent to provide all types of care may be limited by nonadditive costs or by sex-based asymmetries in the costs of particular care types. Using an individual-based simulation, we show that synergistic costs of investing in two tasks or negligible sex-based cost asymmetries select for task specialization and biparental care. Biparental care persists despite intense sexual selection and sex-biased mortality, suggesting that previous models make overly restrictive predictions of the conditions under which cooperation can be maintained. Our model provides a mechanistic underpinning for published models that show that the synergistic benefits of individuals cooperating can stabilize cooperation, both in the context of parental care and in other social scenarios.

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.