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.

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.

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.

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.

Does offspring sex ratio differ between urban and forest populations of great tits (Parus major)?

Since male and female offspring may have different costs and benefits, parents may use sex ratio adjustment to increase their own fitness under different environmental conditions. Urban habitats provide poorer conditions for nestling development in many birds. Therefore, we investigated whether great tits (Parus major) produce different brood sex ratios in urban and natural habitats. We determined the sex of nestlings of 126 broods in two urban and two forest sites between 2012 and 2014 by molecular sexing. We found that brood sex ratio did not differ significantly between urban and forest habitats either at egg-laying or near fledging. Male offspring were larger than females in both habitats. This latter result suggests that male offspring may be more costly to raise than females, yet our findings suggest that urban great tits do not produce more daughters despite the unfavourable breeding conditions. This raises the possibility that other aspects of urban life, such as better post-fledging survival, might favour males and thereby compensate for the extra energetic costs of producing male offspring.

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.

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.

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).

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.

Effects of extreme weather on reproductive success in a temperate-breeding songbird.

The frequency of extreme meteorological events such as heat waves and rainstorms is predicted to increase with climate change. However, there is still little information about how extreme weather influences reproduction in animals. It may not only affect breeding success but might also alter offspring sex ratio if males and females are differentially sensitive to meteorological conditions during development. We investigated the relationship between meteorological conditions and reproductive success over 6 years in a house sparrow population in central Europe. We found that hatching success increased with the number of extremely hot days (daily maximum >31°C) and decreased with the number of extremely cold days (<16°C) during incubation, although the latter effect held only for clutches with relatively short incubation periods. Fledging success was unrelated to weather variables. However, the frequency of extremely hot days had a negative effect on fledglings' body mass and tarsus length, although both of these traits were positively related to average temperature. Additionally, fledglings' body mass increased with the length of period without rainfall before fledging. Male to female ratio among fledglings did not differ from 1:1 and did not vary with weather variables. The magnitude of the effects of extreme meteorological events was usually small, although in some cases comparable to those of ecologically relevant predictors of reproductive success. Our results indicate that meteorological conditions have complex effects on breeding success, as the effects of extreme weather can differ between different aspects of reproduction and also from the effects of overall meteorological conditions.