Signatures of natural selection in the mitochondrial genomes of Tachycineta swallows and their implications for latitudinal patterns of the ‘pace of life’

Latitudinal variation in avian life histories can be summarized as a slow–fast continuum, termed the ‘pace of life’, that encompasses patterns in life span, reproduction, and rates of development among tropical and temperate species. Much of the variation in avian pace of life is tied to differences in rates of long-term metabolic energy expenditure. Given the vital role of the mitochondrion in metabolic processes, studies of variation in the mitochondrial genome may offer opportunities to establish mechanistic links between genetic variation and latitudinal ‘pace of life’ patterns. Using comparative genomic analyses, we examined complete mitochondrial genome sequences obtained from nine, broadly distributed Tachycineta swallow species to test for signatures of natural selection across the mitogenome within a phylogenetic framework. Our results show that although purifying selection is the dominant selective force acting on the mitochondrial genome in Tachycineta, three mitochondrial genes (ND2, ND5, and CYTB) contain regions that exhibit signatures of diversifying selection. Two of these genes (ND2 and ND5) encode interacting subunits of NADH dehydrogenase, and amino residues that were inferred to be targets of positive selection were disproportionately concentrated in these genes. Moreover, the positively selected sites exhibited a phylogenetic pattern that could be indicative of adaptive divergence between “fast” and “slow” lineages. These results suggest that functional variation in cytochrome b and NADH dehydrogenase could mechanistically contribute to latitudinal ‘pace of life’ patterns in Tachycineta.     

Should dispersers be fast learners? Modeling the role of cognition in dispersal syndromes

Both cognitive abilities and dispersal tendencies can vary strongly between individuals. Since cognitive abilities may help dealing with unknown circumstances, it is conceivable that dispersers may rely more heavily on learning abilities than residents. However, cognitive abilities are costly and leaving a familiar place might result in losing the advantage of having learned to deal with local conditions. Thus, individuals which invested in learning to cope with local conditions may be better off staying at their natal place. In order to disentangle the complex relationship between dispersal and learning abilities, we implemented individual‐based simulations. By allowing for developmental plasticity, individuals could either become a ''resident'' or ''dispersal'' cognitive phenotype. The model showed that in general residents have higher learning abilities than dispersers. Dispersers evolve higher learning ability than residents when dispersers have long life spans and when dispersal occurs either early or late in life, thereby maximizing the time in one habitat patch. Time is crucial here, because the longer an individual resides in a location where it can use its learned knowledge or behavior, the more often it profits from it and thus eventually obtains a net benefit from its investment into learning. Both, longevity and the timing of dispersal within lifecycles determine the time individuals have to recoup that investment and thus crucially influence this correlation. We therefore suggest that species'' life history will strongly impact the expected cognitive abilities of dispersers, relative to their resident conspecifics, and that cognitive abilities might be an integral part of dispersal syndromes.     

The evolution of body size in birds. II. The role of reproductive power

Given that body mass evolves non-randomly in birds, it is important to ask what factors might be responsible. One suggestion is that the rate at which individuals turn resources into offspring, termed reproductive power, might explain this non-randomness. This is because, in mammals, the body mass with the highest reproductive power is the most common (modal) one. Reproductive power was estimated for birds from data on energetic content of eggs and population productivity. According to the formulation of Brown et al. (1993), reproductive power is composed of two component processes: acquisition (acquiring resources and storing them in reproductive biomass) and conversion (converting reproductive biomass into offspring). As with mammals, estimates of reproductive power indicate that the most common body mass in birds is also the body mass that maximizes reproductive power. The relationship between reproductive power and diversity is different for species smaller than this modal body mass when compared to those that are larger. The relationship of body mass and reproductive power is different between birds and mammals in two ways: (1) the body mass that maximizes reproductive power is smaller in birds (33g) than in mammals (100g), and (2) mammals generate more reproductive power than an equivalent-sized bird. Reproductive power is determined primarily by acquisition in small birds and mammals, while it is determined by conversion in the largest birds and mammals. It is likely that reproductive power is closely tied to the evolution and diversification of body masses because it constrains the ways in which traits affecting fitness can evolve.     

What lies beneath? Population dynamics conceal pace‐of‐life and sex ratio variation,with implications for resilience to environmental change

Life‐history and pace‐of‐life syndrome theory predict that populations are comprised of individuals exhibiting different reproductive schedules and associated behavioural and physiological traits, optimized to prevailing social and environmental factors. Changing weather and social conditions provide in situ cues altering this life‐history optimality; nevertheless, few studies have considered how tactical, sex‐specific plasticity over an individual's lifespan varies in wild populations and influences population resilience. We examined the drivers of individual life‐history schedules using 31 years of trapping data and 28 years of pedigree for the European badger (Meles meles L.), a long‐lived, iteroparous, polygynandrous mammal that exhibits heterochrony in the timing of endocrinological puberty in male cubs. Our top model for the effects of environmental (social and weather) conditions during a badger's first year on pace‐of‐life explained <10% of variance in the ratio of fertility to age at first reproduction (F/α) and lifetime reproductive success. Conversely, sex ratio (SR) and sex‐specific density explained 52.8% (males) and 91.0% (females) of variance in adult F/α ratios relative to the long‐term population median F/α. Weather primarily affected the sexes at different life‐history stages, with energy constraints limiting the onset of male reproduction but playing a large role in female strategic energy allocation, particularly in relation to ongoing mean temperature increases. Furthermore, the effects of social factors on age of first reproduction and year‐to‐year reproductive success covaried differently with sex, likely due to sex‐specific responses to potential mate availability. For females, low same‐sex densities favoured early primiparity; for males, instead, up to 10% of yearlings successfully mated at high same‐sex densities. We observed substantial SR dynamism relating to differential mortality of life‐history strategists within the population, and propose that shifting ratios of ‘fast’ and ‘slow’ life‐history strategists contribute substantially to population dynamics and resilience to changing conditions.