Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis

Tarka M, Günther A, Niemelae PT, Nakagawa S, Noble DWA. Sex differences in life history, behavior, and physiology along a slow-fast continuum: a meta-analysis. BEHAVIORAL ECOLOGY AND SOCIOBIOLOGY. 2018;72(8): UNSP 132.The pace-of-life syndrome (POLS) hypothesis predicts that behavior and physiology covary with life history. Evidence for such covariation is contradictory, possibly because systematic sources of variation (e.g. sex) have been neglected. Sexes often experience different selection pressures leading to sex-specific allocation between reproduction and self-maintenance, facilitating divergence in life-history. Sex-specific differences in means and possibly variances may therefore play a key role in the POLS framework. We investigate whether sexes differ in means and variances along the fast-slow pace-of-life continuum for life history and physiological and behavioral traits. In addition, we test whether social and environmental characteristics such as breeding strategy, mating system, and study environment explain heterogeneity between the sexes. Using meta-analytic methods, we found that populations with a polygynous mating system or for studies conducted on wild populations, males had a faster pace-of-life for developmental life-history traits (e.g., growth rate), behavior, and physiology. In contrast, adult life-history traits (e.g., lifespan) were shifted towards faster pace-of-life in females, deviating from the other trait categories. Phenotypic variances were similar between the sexes across trait categories and were not affected by mating system or study environment. Breeding strategy did not influence sex differences in variances or means. We discuss our results in the light of sex-specific selection that might drive sex-specific differences in pace-of-life and ultimately POLS

Estimating Heritabilities and Genetic Correlations: Comparing the ‘Animal Model’ with Parent-Offspring Regression Using Data from a Natural Population

Quantitative genetic parameters are nowadays more frequently estimated with restricted maximum likelihood using the ‘animal model’ than with traditional methods such as parent-offspring regressions. These methods have however rarely been evaluated using equivalent data sets. We compare heritabilities and genetic correlations from animal model and parent-offspring analyses, respectively, using data on eight morphological traits in the great reed warbler (Acrocephalus arundinaceus). Animal models were run using either mean trait values or individual repeated measurements to be able to separate between effects of including more extended pedigree information and effects of replicated sampling from the same individuals. We show that the inclusion of more pedigree information by the use of mean traits animal models had limited effect on the standard error and magnitude of heritabilities. In contrast, the use of repeated measures animal model generally had a positive effect on the sampling accuracy and resulted in lower heritabilities; the latter due to lower additive variance and higher phenotypic variance. For most trait combinations, both animal model methods gave genetic correlations that were lower than the parent-offspring estimates, whereas the standard errors were lower only for the mean traits animal model. We conclude that differences in heritabilities between the animal model and parent-offspring regressions were mostly due to the inclusion of individual replicates to the animal model rather than the inclusion of more extended pedigree information. Genetic correlations were, on the other hand, primarily affected by the inclusion of more pedigree information. This study is to our knowledge the most comprehensive empirical evaluation of the performance of the animal model in relation to parent-offspring regressions in a wild population. Our conclusions should be valuable for reconciliation of data obtained in earlier studies as well as for future meta-analyses utilizing estimates from both traditional methods and the animal model

Hybridization but No Evidence for Backcrossing and Introgression in a Sympatric Population of Great Reed Warblers and Clamorous Reed Warblers

Hybridization is observed frequently in birds, but often it is not known whether the hybrids are fertile and if backcrossing occurs. The breeding ranges of the great reed warbler (Acrocephalus arundinaceus) and the clamorous reed warbler (A. stentoreus) overlap in southern Kazakhstan and a previous study has documented hybridization in a sympatric population. In the present study, we first present a large set of novel microsatellite loci isolated and characterised in great reed warblers. Secondly, we evaluate whether hybridization in the sympatric breeding population has been followed by backcrossing and introgression

Postglacial Colonisation Patterns and the Role of Isolation and Expansion in Driving Diversification in a Passerine Bird

Pleistocene glacial cycles play a major role in diversification and speciation, although the relative importance of isolation and expansion in driving diversification remains debated. We analysed mitochondrial DNA sequence data from 15 great reed warbler (Acrocephalus arundinaceus) populations distributed over the vast Eurasian breeding range of the species, and revealed unexpected postglacial expansion patterns from two glacial refugia. There were 58 different haplotypes forming two major clades, A and B. Clade A dominated in Western Europe with declining frequencies towards Eastern Europe and the Middle East, but showed a surprising increase in frequency in Western and Central Asia. Clade B dominated in the Middle East, with declining frequencies towards north in Central and Eastern Europe and was absent from Western Europe and Central Asia. A parsimonious explanation for these patterns is independent postglacial expansions from two isolated refugia, and mismatch distribution analyses confirmed this suggestion. Gene flow analyses showed that clade A colonised both Europe and Asia from a refugium in Europe, and that clade B expanded much later and colonised parts of Europe from a refugium in the Middle East. Great reed warblers in the eastern parts of the range have slightly paler plumage than western birds (sometimes treated as separate subspecies; A. a. zarudnyi and A. a. arundinaceus, respectively) and our results suggest that the plumage diversification took place during the easterly expansion of clade A. This supports the postglacial expansion hypothesis proposing that postglacial expansions drive diversification in comparatively short time periods. However, there is no indication of any (strong) reproductive isolation between clades and our data show that the refugia populations became separated during the last glaciation. This is in line with the Pleistocene speciation hypothesis invoking that much longer periods of time in isolation are needed for speciation to occur

Adaptive responses of animals to climate change are most likely insufficient

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species. © 2019, The Author(s)

Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms

Sex differences in life history, physiology, and behavior are nearly ubiquitous across taxa, owing to sex-specific selection that arises from different reproductive strategies of the sexes. The pace-of-life syndrome (POLS) hypothesis predicts that most variation in such traits among individuals, populations, and species falls along a slow-fast pace-of-life continuum. As a result of their different reproductive roles and environment, the sexes also commonly differ in pace-of-life, with important consequences for the evolution of POLS. Here, we outline mechanisms for how males and females can evolve differences in POLS traits and in how such traits can covary differently despite constraints resulting from a shared genome. We review the current knowledge of the genetic basis of POLS traits and suggest candidate genes and pathways for future studies. Pleiotropic effects may govern many of the genetic correlations, but little is still known about the mechanisms involved in trade-offs between current and future reproduction and their integration with behavioral variation. We highlight the importance of metabolic and hormonal pathways in mediating sex differences in POLS traits; however, there is still a shortage of studies that test for sex specificity in molecular effects and their evolutionary causes. Considering whether and how sexual dimorphism evolves in POLS traits provides a more holistic framework to understand how behavioral variation is integrated with life histories and physiology, and we call for studies that focus on examining the sex-specific genetic architecture of this integration

Adaptive responses of animals to climate change are most likely insufficient

Biological responses to climate change have been widely documented across taxa and regions, but it remains unclear whether species are maintaining a good match between phenotype and environment, i.e. whether observed trait changes are adaptive. Here we reviewed 10,090 abstracts and extracted data from 71 studies reported in 58 relevant publications, to assess quantitatively whether phenotypic trait changes associated with climate change are adaptive in animals. A meta-analysis focussing on birds, the taxon best represented in our dataset, suggests that global warming has not systematically affected morphological traits, but has advanced phenological traits. We demonstrate that these advances are adaptive for some species, but imperfect as evidenced by the observed consistent selection for earlier timing. Application of a theoretical model indicates that the evolutionary load imposed by incomplete adaptive responses to ongoing climate change may already be threatening the persistence of species.Peer reviewe

Evolutionary dynamics of migration and breeding in wild birds: genetic architecture, sexual conflicts and evolutionary constraints

Our knowledge of the evolutionary potential of traits involved in different selective episodes, especially in natural populations, is still limited. This is true for questions such as the genetic basis and inheritance of traits, how natural and sexual selection acts on them, and how selective conflicts influence the evolutionary response to selection. In my thesis, I investigate these questions, using a long term study population of great reed warblers (Acrocephalus arundinaceus) with known pedigree, as a model system. I have focused on traits at the interface between migration and breeding and worked both in the field, the DNA lab and used powerful statistical tools in quantitative genetics and quantitative trait locus (QTL) mapping. Moreover, using new technology (geolocators), I describe full migratory paths showing a unique case of small songbirds flying rapidly (probably non-stop), over the Mediterranean Sea and the Sahara Desert, where after birds spread out to winter over a huge range covering the entire sub-Saharan West Africa to the Congo Basin in the east. Early spring arrival to the breeding site is decisive for breeding success in song birds. I found that arrival date is a heritable trait, with higher genetic variance in experienced (≥ 2 year old) as compared with inexperienced (1 year old) birds. Traits are not independent units which can constrain their evolution. However, I found no sign of a morphological ‘migratory syndrome’ (genetic correlations between migration traits) on the population level, and no evolutionary constraint acting through morphology on arrival date. Wing length was negatively correlated with arrival. I found a strong intralocus sexual conflict acting on wing length, where males are selected for long wings and females for short wings. Also I present a large-effect QTL for wing length located on chromosome 2, which recently has been confirmed in the zebra finch, suggesting its generality among birds. I also present a conceptual framework for the study of intralocus sexual conflict. An analysis of 13 traits suggested that traits within a population can be in very different stages of the conflict. I have also investigated potential evolutionary constraints through genetic correlations between traits in ten long-term study populations of wild birds and found evolutionary constraints on morphology, but mainly on current selection. Finally I investigate a potential source of genetic variation in a hybrid zone between great reed warblers and clamorous warblers (A. stentoreus). No sign of introgression was found, suggesting that hybrids are sterile or offspring inviable. These studies make an important contribution to our knowledge of evolutionary dynamics in the wild

Selection and evolutionary potential of spring arrival phenology in males and females of a migratory songbird

The timing of annual life-history events affects survival and reproduction of all organisms. A changing environment can perturb phenological adaptations and an important question is if populations can evolve fast enough to track the environmental changes. Yet, little is known about selection and evolutionary potential of traits determining the timing of crucial annual events. Migratory species, which travel between different climatic regions, are particularly affected by global environmental changes. To increase our understanding of evolutionary potential and selection of timing traits, we investigated the quantitative genetics of arrival date at the breeding ground using a multigenerational pedigree of a natural great reed warbler (Acrocephalus arundinaceus) population. We found significant heritability of 16.4% for arrival date and directional selection for earlier arrival in both sexes acting through reproductive success, but not through lifespan. Mean arrival date advanced with 6days over 20years, which is in exact accordance with our predicted evolutionary response based on the breeder's equation. However, this phenotypic change is unlikely to be caused by microevolution, because selection seems mainly to act on the nongenetic component of the trait. Furthermore, demographical changes could also not account for the advancing arrival date. Instead, a strong correlation between spring temperatures and population mean arrival date suggests that phenotypic plasticity best explains the advancement of arrival date in our study population. Our study dissects the evolutionary and environmental forces that shape timing traits and thereby increases knowledge of how populations cope with rapidly changing environments