AVONET: morphological, ecological and geographical data for all birds.

Functional traits offer a rich quantitative framework for developing and testing theories in evolutionary biology, ecology and ecosystem science. However, the potential of functional traits to drive theoretical advances and refine models of global change can only be fully realised when species-level information is complete. Here we present the AVONET dataset containing comprehensive functional trait data for all birds, including six ecological variables, 11 continuous morphological traits, and information on range size and location. Raw morphological measurements are presented from 90,020 individuals of 11,009 extant bird species sampled from 181 countries. These data are also summarised as species averages in three taxonomic formats, allowing integration with a global phylogeny, geographical range maps, IUCN Red List data and the eBird citizen science database. The AVONET dataset provides the most detailed picture of continuous trait variation for any major radiation of organisms, offering a global template for testing hypotheses and exploring the evolutionary origins, structure and functioning of biodiversity.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family.

Extra-pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.

The couple that sings together stays together: duetting, aggression and extra-pair paternity in a promiscuous bird species.

When individuals mate outside the pair bond, males should employ behaviours such as aggression or vocal displays (e.g. duetting) that help assure paternity of the offspring they care for. We tested whether male paternity was associated with aggression or duetting in the red-backed fairy-wren, a species exhibiting high rates of extra-pair paternity. During simulated territorial intrusions, aggression and duetting were variable among and repeatable within males, suggesting behavioural consistency of individuals. Males with quicker and stronger duet responses were cuckolded less often than males with slower and weaker responses. In contrast, physical aggression was not correlated with male paternity. These results suggest that either acoustic mate guarding or male-female vocal negotiations via duetting lead to increased paternity assurance, whereas physical aggression does not.

The role of ecological variation in driving divergence of sexual and non-sexual traits in the red-backed fairy-wren (Malurus melanocephalus).

BACKGROUND: Many species exhibit geographic variation in sexual signals, and divergence in these traits may lead to speciation. Sexual signals may diverge due to differences in ecology if the environment constrains signal production or transmission. Alternatively, sexual signals may diverge stochastically through sexual selection or genetic drift, with little environmental influence. To distinguish between these alternatives we quantified variation in two putative sexual signals--tail length and plumage color--and a suite of non-sexual morphometric traits across the geographic range of the red-backed fairy-wren (Malurus melanocephalus). We then tested for associations between these traits and a number of environmental variables using generalized dissimilarity models. RESULTS: Variation in morphometric traits was explained well by environmental variation, irrespective of geographic distance between sites. Among putative signals, variation in plumage color was best explained by geographic distance, whereas tail length was best explained by environmental variation. Divergence in male plumage color was not coincident with the boundary between genetic lineages, but was greatest across a contact zone located 300 km east of the genetic boundary. CONCLUSIONS: Morphometric traits describing size and shape have likely been subject to ecological selection and thus appear to track local environmental variation regardless of subspecies identity. Ecological selection appears to have also influenced the evolution of tail length as a signal, but has played a limited role in shaping geographic variation in plumage color, consistent with stochastic divergence in concert with Fisherian selection on this trait. The lack of coincidence between the genetic boundary and the contact zone between plumage types suggests that the sexual plumage signal of one subspecies has introgressed into the genetic background of the other. Thus, this study provides insight into the various ways in which signal evolution may occur within a species, and the geographic patterns of signal variation that can arise, especially following secondary contact.

Experimental evidence that extra-pair mating drives asymmetrical introgression of a sexual trait.

Theory suggests that traits under positive selection may introgress asymmetrically across a hybrid zone, potentially driven by sexual selection. Two subspecies of the red-backed fairy-wren (Malurus melanocephalus) differ primarily in a sexual signal used in mate choice-red versus orange male back plumage colour-but phylogeographic analyses suggest asymmetrical introgression of red plumage into the genetic background of the orange subspecies. We hypothesized that this asymmetrical introgression may be facilitated by sexual selection if red males have a mating advantage over orange males. We tested this hypothesis with correlational data and a plumage manipulation experiment where we reddened the back plumage of a subset of orange males to mimic males of the red subspecies. There was no correlational evidence of a mating advantage to naturally redder males in this population. Experimentally reddened males sired a similar amount of within-pair young and lost paternity at the same rate as orange males, but they sired significantly more extra-pair young, leading to substantially higher total reproductive success. Thus, we conclude that sexual selection via extra-pair mating is a likely mechanism responsible for the asymmetrical introgression of plumage colour in this system, and is potentially driven by a sensory bias for the red plumage signal.

Sperm Numbers as a Paternity Guard in a Wild Bird.

Sperm competition is thought to impose strong selection on males to produce competitive ejaculates to outcompete rival males under competitive mating conditions. Our understanding of how different sperm traits influence fertilization success, however, remains limited, especially in wild populations. Recent literature highlights the importance of incorporating multiple ejaculate traits and pre-copulatory sexually selected traits in analyses aimed at understanding how selection acts on sperm traits. However, variation in a male's ability to gain fertilization success may also depend upon a range of social and ecological factors that determine the opportunity for mating events both within and outside of the social pair-bond. Here, we test for an effect of sperm quantity and sperm size on male reproductive success in the red-back fairy-wren (Malurus melanocephalus) while simultaneously accounting for pre-copulatory sexual selection and potential socio-ecological correlates of male mating success. We found that sperm number (i.e., cloacal protuberance volume), but not sperm morphology, was associated with reproductive success in male red-backed fairy-wrens. Most notably, males with large numbers of sperm available for copulation achieved greater within-pair paternity success. Our results suggest that males use large sperm numbers as a defensive strategy to guard within-pair paternity success in a system where there is a high risk of sperm competition and female control of copulation. Finally, our work highlights the importance of accounting for socio-ecological factors that may influence male mating opportunities when examining the role of sperm traits in determining male reproductive success.

Is there convergence of gut microbes in blood-feeding vertebrates?

Animal microbiomes play an important role in dietary adaptation, yet the extent to which microbiome changes exhibit parallel evolution is unclear. Of particular interest is an adaptation to extreme diets, such as blood, which poses special challenges in its content of proteins and lack of essential nutrients. In this study, we assessed taxonomic signatures (by 16S rRNA amplicon profiling) and potential functional signatures (inferred by Phylogenetic Investigation of Communities by Reconstruction of Unobserved States (PICRUSt)) of haematophagy in birds and bats. Our goal was to test three alternative hypotheses: no convergence of microbiomes, convergence in taxonomy and convergence in function. We find a statistically significant effect of haematophagy in terms of microbial taxonomic convergence across the blood-feeding bats and birds, although this effect is small compared to the differences found between haematophagous and non-haematophagous species within the two host clades. We also find some evidence of convergence at the predicted functional level, although it is possible that the lack of metagenomic data and the poor representation of microbial lineages adapted to haematophagy in genome databases limit the power of this approach. The results provide a paradigm for exploring convergent microbiome evolution replicated with independent contrasts in different host lineages. This article is part of the theme issue 'Convergent evolution in the genomics era: new insights and directions'.

The gut of the finch: uniqueness of the gut microbiome of the Galápagos vampire finch.

BACKGROUND: Darwin's finches are a clade of 19 species of passerine birds native to the Galápagos Islands, whose biogeography, specialized beak morphologies, and dietary choices-ranging from seeds to blood-make them a classic example of adaptive radiation. While these iconic birds have been intensely studied, the composition of their gut microbiome and the factors influencing it, including host species, diet, and biogeography, has not yet been explored. RESULTS: We characterized the microbial community associated with 12 species of Darwin's finches using high-throughput 16S rRNA sequencing of fecal samples from 114 individuals across nine islands, including the unusual blood-feeding vampire finch (Geospiza septentrionalis) from Darwin and Wolf Islands. The phylum-level core gut microbiome for Darwin's finches included the Firmicutes, Gammaproteobacteria, and Actinobacteria, with members of the Bacteroidetes at conspicuously low abundance. The gut microbiome was surprisingly well conserved across the diversity of finch species, with one exception-the vampire finch-which harbored bacteria that were either absent or extremely rare in other finches, including Fusobacterium, Cetobacterium, Ureaplasma, Mucispirillum, Campylobacter, and various members of the Clostridia-bacteria known from the guts of carnivorous birds and reptiles. Complementary stable isotope analysis of feathers revealed exceptionally high δ15N isotope values in the vampire finch, resembling top marine predators. The Galápagos archipelago is also known for extreme wet and dry seasons, and we observed a significant seasonal shift in the gut microbial community of five additional finch species sampled during both seasons. CONCLUSIONS: This study demonstrates the overall conservatism of the finch gut microbiome over short (< 1 Ma) divergence timescales, except in the most extreme case of dietary specialization, and elevates the evolutionary importance of seasonal shifts in driving not only species adaptation, but also gut microbiome composition.

Differential rates of phenotypic introgression are associated with male behavioral responses to multiple signals.

Sexual selection on multiple signals may lead to differential rates of signal introgression across hybrid zones if some signals contribute to reproductive isolation but others facilitate gene flow. Competition among males is one powerful form of sexual selection, but male behavioral responses to multiple traits have not been considered in a system where traits have introgressed differentially. Using playbacks, mounts, and a reciprocal experimental design, we tested the hypothesis that male responses to song and plumage in two subspecies of red-backed fairy-wren (Malurus melanocephalus) explain patterns of differential signal introgression (song has not introgressed, whereas plumage color has introgressed asymmetrically). We found that males of both subspecies discriminated symmetrically between subspecies' songs at a long range, but at a close range, we found that aggression was equal for both subspecies' plumage and songs. Taken together, our results suggest that male behavioral responses hinder the introgression of song, but allow for the observed asymmetrical introgression of plumage. Our results highlight how behavioral responses are a key component of signal evolution when recently divergent taxa come together, and how differential responses to multiple signals may lead to differential signal introgression and novel trait combinations.

Genomic and morphological analysis of a semipermeable avian hybrid zone suggests asymmetrical introgression of a sexual signal.

Hybrid zones are geographic regions where differentiated taxa meet and potentially exchange genes. Increasingly, genomic analyses have demonstrated that many hybrid zones are semipermeable boundaries across which introgression is highly variable. In some cases, certain alleles penetrate across the hybrid zone in only one direction, recombining into the alternate genome. We investigated this phenomenon using genomic (genotyping-by-sequencing) and morphological (plumage reflectance spectrophotometry) analyses of the hybrid zone between two subspecies of the red-backed fairy-wren (Malurus melanocephalus) that differ conspicuously in a sexual signal, male back plumage color. Geographic cline analyses revealed a highly variable pattern of differential introgression, with many narrow coincident clines combined with several significantly wider clines, suggesting that the hybrid zone is a semipermeable tension zone. The plumage cline was shifted significantly into the genomic background of the orange subspecies, consistent with sexual selection driving asymmetrical introgression of red plumage alleles across the hybrid zone. This interpretation is supported by previous experimental work demonstrating an extra-pair mating advantage for red males, but the role of genetic dominance in driving this pattern remains unclear. This study highlights the potential for sexual selection to erode taxonomic boundaries and promote gene flow, particularly at an intermediate stage of divergence.