Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species.

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constrains symbiont populations. We parameterized metabolic theory equations to investigate how bird species' body size and the body size of their feather mites relate to mite abundance according to four potential energy (uropygial gland size) and space constraints (wing area, total length of barbs and number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance across 106 passerine bird species (26,604 individual birds sampled), using phylogenetic modelling and quantile regression. Feather mite abundance was strongly constrained by host space (number of feather barbs) but not by energy. Moreover, feather mite species' body size was unrelated to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

High frequency of social polygyny reveals little costs for females in a songbird.

Mating system theory predicts that social polygyny-when one male forms pair bonds with two females-may evolve by female choice in species with biparental care. Females will accept a polygynous male if the benefit of mating with a male providing high-quality genes or rearing resources outweighs the cost of sharing mate assistance in parental care. Based on this rationale, we hypothesise that the population frequency of social polygyny (FSP) varies due to changes in mate sharing costs caused by changing environmental conditions. We predicted that: (1) polygamous females (i.e. mated with a polygynous male) pay a survival cost compared to monogamous females; (2) FSP would be higher in years with better rearing conditions and (3) the difference in survival rates between monogamous and polygamous females would be small following years with higher FSP. We tested these predictions using regression and multistate analyses of capture-recapture data of pied flycatchers, Ficedula hypoleuca, in central Spain collected over 26 years (1990-2016). Monogamous females had a higher mean survival rate than polygamous females (prediction 1), but there was no difference in survival between polygynous and monogamous males. In addition, FSP was positively associated with annual reproductive success (a proxy of the quality of rearing conditions-prediction 2). Finally, following years with high FSP, the survival of polygamous females was similar to that of monogamous females (prediction 3), while the chance of breeding in a polygamous state for 2 years in a row increased for both males and females. Our findings suggest that fluctuating environmental conditions may be a necessary but neglected aspect of understanding social polygyny mechanisms.

Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers.

Speciation is a continuous process during which genetic changes gradually accumulate in the genomes of diverging species. Recent studies have documented highly heterogeneous differentiation landscapes, with distinct regions of elevated differentiation ("differentiation islands") widespread across genomes. However, it remains unclear which processes drive the evolution of differentiation islands; how the differentiation landscape evolves as speciation advances; and ultimately, how differentiation islands are related to speciation. Here, we addressed these questions based on population genetic analyses of 200 resequenced genomes from 10 populations of four Ficedula flycatcher sister species. We show that a heterogeneous differentiation landscape starts emerging among populations within species, and differentiation islands evolve recurrently in the very same genomic regions among independent lineages. Contrary to expectations from models that interpret differentiation islands as genomic regions involved in reproductive isolation that are shielded from gene flow, patterns of sequence divergence (d(xy) and relative node depth) do not support a major role of gene flow in the evolution of the differentiation landscape in these species. Instead, as predicted by models of linked selection, genome-wide variation in diversity and differentiation can be explained by variation in recombination rate and the density of targets for selection. We thus conclude that the heterogeneous landscape of differentiation in Ficedula flycatchers evolves mainly as the result of background selection and selective sweeps in genomic regions of low recombination. Our results emphasize the necessity of incorporating linked selection as a null model to identify genome regions involved in adaptation and speciation.

Evolutionary analysis of the female-specific avian W chromosome.

The typically repetitive nature of the sex-limited chromosome means that it is often excluded from or poorly covered in genome assemblies, hindering studies of evolutionary and population genomic processes in non-recombining chromosomes. Here, we present a draft assembly of the non-recombining region of the collared flycatcher W chromosome, containing 46 genes without evidence of female-specific functional differentiation. Survival of genes during W chromosome degeneration has been highly non-random and expression data suggest that this can be attributed to selection for maintaining gene dose and ancestral expression levels of essential genes. Re-sequencing of large population samples revealed dramatically reduced levels of within-species diversity and elevated rates of between-species differentiation (lineage sorting), consistent with low effective population size. Concordance between W chromosome and mitochondrial DNA phylogenetic trees demonstrates evolutionary stable matrilineal inheritance of this nuclear-cytonuclear pair of chromosomes. Our results show both commonalities and differences between W chromosome and Y chromosome evolution.

Using the BirdTree.org website to obtain robust phylogenies for avian comparative studies: A primer.

Comparative studies of trait evolution require accounting for the shared evolutionary history. This is done by including phylogenetic hypotheses into statistical analyses of species' traits, for which birds often serve as excellent models. The online publication of the most complete molecular phylogeny of extant bird species (www.birdtree.org, BirdTree hereafter) now allows evolutionary biologists to rapidly obtain sets of equally plausible phylogenetic trees for any set of species to be incorporated as a phylogenetic hypothesis in comparative analyses. We discuss methods to use BirdTree tree sets for comparative studies, either by building a consensus tree that can be incorporated into standard comparative analyses, or by using tree sets to account for the effect of phylogenetic uncertainty. Methods accounting for phylogenetic uncertainty should be preferred whenever possible because they should provide more reliable parameter estimates and realistic confidence intervals around them. Based on a real comparative dataset, we ran simulations to investigate the effect of variation in the size of the random tree sets downloaded from BirdTree on the variability of parameter estimates from a bivariate relationship between mass-specific productivity and body mass. Irrespective of the method of analysis, using at least 1,000 trees allows obtaining parameter estimates with very small (< 0.15%) coefficients of variation. We argue that BirdTree, due to the ease of use and the major advantages over previous 'traditional' methods to obtain phylogenetic hypotheses of bird species (e.g. supertrees or manual coding of published phylogenies), will become the standard reference in avian comparative studies for years to come.

No personality without experience? A test on Rana dalmatina tadpoles.

While the number of studies reporting the presence of individual behavioral consistency (animal personality, behavioral syndrome) has boomed in the recent years, there is still much controversy about the proximate and ultimate mechanisms resulting in the phenomenon. For instance, direct environmental effects during ontogeny (phenotypic plasticity) as the proximate mechanism behind the emergence of consistent individual differences in behavior are usually overlooked compared to environmental effects operating across generations (genetic adaptation). Here, we tested the effects of sociality and perceived predation risk during ontogeny on the strength of behavioral consistency in agile frog (Rana dalmatina) tadpoles in a factorial common garden experiment. Tadpoles reared alone and without predatory cues showed zero repeatability within (i.e., lack of personality) and zero correlation between (i.e., lack of syndrome) activity and risk-taking. On the other hand, cues from predators alone induced both activity and risk-taking personalities, while cues from predators and conspecifics together resulted in an activity - risk-taking behavioral syndrome. Our results show that individual experience has an unequivocal role in the emergence of behavioral consistency. In this particular case, the development of behavioral consistency was most likely the result of genotype × environment interactions, or with other words, individual variation in behavioral plasticity.

The relationship between DRD4 polymorphisms and phenotypic correlations of behaviors in the collared flycatcher.

There is increasing evidence that the genetic architecture of exploration behavior includes the dopamine receptor D4 gene (DRD4). Such a link implies that the within-individual consistency in the same behavior has a genetic basis. Behavioral consistency is also prevalent in the form of between-individual correlation of functionally different behaviors; thus, the relationship between DRD4 polymorphism and exploration may also be manifested for other behaviors. Here, in a Hungarian population of the collared flycatcher, Ficedula albicollis, we investigate how males with distinct DRD4 genotypes differ in the consistent elements of their behavioral displays during the courtship period. In completely natural conditions, we assayed novelty avoidance, aggression and risk-taking, traits that were previously shown repeatable over time and correlate with each other, suggesting that they could have a common mechanistic basis. We identified two single-nucleotide polymorphisms (SNP554 and SNP764) in the exon 3 of the DRD4 gene by sequencing a subsample, then we screened 202 individuals of both sexes for these SNPs. Focusing on the genotypic variation in courting males, we found that "AC" heterozygote individuals at the SNP764 take lower risk than the most common "AA" homozygotes (the "CC" homozygotes were not represented in our subsample of males). We also found a considerable effect size for the relationship between SNP554 polymorphism and novelty avoidance. Therefore, in addition to exploration, DRD4 polymorphisms may also be associated with the regulation of behaviors that may incur fear or stress. Moreover, polymorphisms at the two SNPs were not independent indicating a potential role for genetic constraints or another functional link, which may partially explain behavioral correlations.

Assessing the effects of climate on host-parasite interactions: a comparative study of European birds and their parasites.

BACKGROUND: Climate change potentially has important effects on distribution, abundance, transmission and virulence of parasites in wild populations of animals. METHODOLOGY/PRINCIPAL FINDING: Here we analyzed paired information on 89 parasite populations for 24 species of bird hosts some years ago and again in 2010 with an average interval of 10 years. The parasite taxa included protozoa, feather parasites, diptera, ticks, mites and fleas. We investigated whether change in abundance and prevalence of parasites was related to change in body condition, reproduction and population size of hosts. We conducted analyses based on the entire dataset, but also on a restricted dataset with intervals between study years being 5-15 years. Parasite abundance increased over time when restricting the analyses to datasets with an interval of 5-15 years, with no significant effect of changes in temperature at the time of breeding among study sites. Changes in host body condition and clutch size were related to change in temperature between first and second study year. In addition, changes in clutch size, brood size and body condition of hosts were correlated with change in abundance of parasites. Finally, changes in population size of hosts were not significantly related to changes in abundance of parasites or their prevalence. CONCLUSIONS/SIGNIFICANCE: Climate change is associated with a general increase in parasite abundance. Variation in laying date depended on locality and was associated with latitude while body condition of hosts was associated with a change in temperature. Because clutch size, brood size and body condition were associated with change in parasitism, these results suggest that parasites, perhaps mediated through the indirect effects of temperature, may affect fecundity and condition of their hosts. The conclusions were particularly in accordance with predictions when the restricted dataset with intervals of 5-15 years was used, suggesting that short intervals may bias findings.

Do animals living in larger groups experience greater parasitism? A meta-analysis.

Parasitism is widely viewed as the primary cost of sociality and a constraint on group size, yet studies report varied associations between group size and parasitism. Using the largest database of its kind, we performed a meta-analysis of 69 studies of the relationship between group size and parasite risk, as measured by parasitism and immune defenses. We predicted a positive correlation between group size and parasitism with organisms that show contagious and environmental transmission and a negative correlation for searching parasites, parasitoids, and possibly vector-borne parasites (on the basis of the encounter-dilution effect). Overall, we found a positive effect of group size (r = 0.187) that varied in magnitude across transmission modes and measures of parasite risk, with only weak indications of publication bias. Among different groups of hosts, we found a stronger relationship between group size and parasite risk in birds than in mammals, which may be driven by ecological and social factors. A metaregression showed that effect sizes increased with maximum group size. Phylogenetic meta-analyses revealed no evidence for phylogenetic signal in the strength of the group size-parasitism relationship. We conclude that group size is a weak predictor of parasite risk except in species that live in large aggregations, such as colonial birds, in which effect sizes are larger.

Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review.

Comparative analyses aim to explain interspecific variation in phenotype among taxa. In this context, phylogenetic approaches are generally applied to control for similarity due to common descent, because such phylogenetic relationships can produce spurious similarity in phenotypes (known as phylogenetic inertia or bias). On the other hand, these analyses largely ignore potential biases due to within-species variation. Phylogenetic comparative studies inherently assume that species-specific means from intraspecific samples of modest sample size are biologically meaningful. However, within-species variation is often significant, because measurement errors, within- and between-individual variation, seasonal fluctuations, and differences among populations can all reduce the repeatability of a trait. Although simulations revealed that low repeatability can increase the type I error in a phylogenetic study, researchers only exercise great care in accounting for similarity in phenotype due to common phylogenetic descent, while problems posed by intraspecific variation are usually neglected. A meta-analysis of 194 comparative analyses all adjusting for similarity due to common phylogenetic descent revealed that only a few studies reported intraspecific repeatabilities, and hardly any considered or partially dealt with errors arising from intraspecific variation. This is intriguing, because the meta-analytic data suggest that the effect of heterogeneous sampling can be as important as phylogenetic bias, and thus they should be equally controlled in comparative studies. We provide recommendations about how to handle such effects of heterogeneous sampling.

Correlated evolution of nucleotide substitution rates and allelic variation in Mhc-DRB lineages of primates.

BACKGROUND: The major histocompatibility complex (MHC) is a key model of genetic polymorphism. Selection pressure by pathogens or other microevolutionary forces may result in a high rate of non-synonymous substitutions at the codons specifying the contact residues of the antigen binding sites (ABS), and the maintenance of extreme MHC allelic variation at the population/species level. Therefore, selection forces favouring MHC variability for any reason should cause a correlated evolution between substitution rates and allelic polymorphism. To investigate this prediction, we characterised nucleotide substitution rates and allelic polymorphism (i.e. the number of alleles detected in relation to the number of animals screened) of several Mhc class II DRB lineages in 46 primate species, and tested for a correlation between them. RESULTS: First, we demonstrate that species-specific and lineage-specific evolutionary constraints favour species- and lineage-dependent substitution rate at the codons specifying the ABS contact residues (i.e. certain species and lineages can be characterised by high substitution rate, while others have low rate). Second, we show that although the degree of the non-synonymous substitution rate at the ABS contact residues was systematically higher than the degree of the synonymous substitution rate, these estimates were strongly correlated when we controlled for species-specific and lineage-specific effects, and also for the fact that different studies relied on different sample size. Such relationships between substitution rates of different types could even be extended to the non-contact residues of the molecule. Third, we provide statistical evidence that increased substitution rate along a MHC gene may lead to allelic variation, as a high substitution rate can be observed in those lineages in which many alleles are maintained. Fourth, we show that the detected patterns were independent of phylogenetic constraints. When we used phylogenetic models that control for similarity between species, due to common descent, and focused on variations within a single lineage (DRB1*03), the positive relationship between different substitution rates and allelic polymorphisms was still robust. Finally, we found the same effects to emerge in the analyses that eliminated within-species variation in MHC traits by using strictly single population-level studies. However, in a set of contrasting analyses, in which we focused on the non-functional DRB6 locus, the correlation between substitution rates and allelic variation was not prevalent. CONCLUSION: Our results indicate that positive selection for the generation of allelic polymorphism acting on the functional part of the protein has consequences for the nucleotide substitution rate along the whole exon 2 sequence of the Mhc-DRB gene. Additionally, we proved that an increased substitution rate can promote allelic variation within lineages. Consequently, the evolution of different characteristics of genetic polymorphism is not independent.