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The DNA-binding protein PRDM9 has a critical role in specifying meiotic recombination hotspots in mice and apes, but it appears to be absent from other vertebrate species, including birds. To study the evolution and determinants of recombination in species lacking the gene that encodes PRDM9, we inferred fine-scale genetic maps from population resequencing data for two bird species: the zebra finch, Taeniopygia guttata, and the long-tailed finch, Poephila acuticauda. We found that both species have recombination hotspots, which are enriched near functional genomic elements. Unlike in mice and apes, most hotspots are shared between the two species, and their conservation seems to extend over tens of millions of years. These observations suggest that in the absence of PRDM9, recombination targets functional features that both enable access to the genome and constrain its evolution.

In Himalayan songbirds, the speciation rate is ultimately set by ecological competition, rather than by the rate of acquisition of reproductive isolation. New species need new niches The beginnings of adaptive radiation and speciation have been widely studied — in Darwin's finches, sticklebacks and cichlid fish, for example — but relatively little is known about what happens next. Specifically, what is the rate-limiting step for the establishment of new species? This seven-year study of the 358 songbird species found on the Himalayan slopes suggests that it is the rates at which new niches are created and occupied that limits diversification, not the rate at which new species form through reproductive isolation. Speciation generally involves a three-step process—range expansion, range fragmentation and the development of reproductive isolation between spatially separated populations 1 , 2 . Speciation relies on cycling through these three steps and each may limit the rate at which new species form 1 , 3 . We estimate phylogenetic relationships among all Himalayan songbirds to ask whether the development of reproductive isolation and ecological competition, both factors that limit range expansions 4 , set an ultimate limit on speciation. Based on a phylogeny for all 358 species distributed along the eastern elevational gradient, here we show that body size and shape differences evolved early in the radiation, with the elevational band occupied by a species evolving later. These results are consistent with competition for niche space limiting species accumulation 5 . Even the elevation dimension seems to be approaching ecological saturation, because the closest relatives both inside the assemblage and elsewhere in the Himalayas are on average separated by more than five million years, which is longer than it generally takes for reproductive isolation to be completed 2 , 3 , 6 ; also, elevational distributions are well explained by resource availability, notably the abundance of arthropods, and not by differences in diversification rates in different elevational zones. Our results imply that speciation rate is ultimately set by niche filling (that is, ecological competition for resources), rather than by the rate of acquisition of reproductive isolation.

Most of our understanding of the fundamental processes of mutation and recombination stems from a handful of disparate model organisms and pedigree studies of mammals, with little known about other vertebrates. To gain a broader comparative perspective, we focused on the zebra finch ( Taeniopygia castanotis ), which, like other birds, differs from mammals in its karyotype (which includes many micro-chromosomes), in the mechanism by which recombination is directed to the genome, and in aspects of ontogenesis. We collected genome sequences from three generation pedigrees that provide information about 80 meioses, inferring 202 single-point de novo mutations, 1,088 crossovers, and 275 non-crossovers. On that basis, we estimated a sex-averaged mutation rate of 5.0 × 10 -9 per base pair per generation, on par with mammals that have a similar generation time (~2–3 years). Also as in mammals, we found a paternal germline mutation bias at later stages of gametogenesis (of 1.7:1) but no discernible difference between sexes in early development. Examining recombination patterns, we found that the sex-averaged crossover rate on macro-chromosomes is 0.93 cM/Mb, with a pronounced enrichment of crossovers near telomeres. In contrast, non-crossover rates are more uniformly distributed. On micro-chromosomes, sex-averaged crossover rates are substantially higher (3.96 cM/Mb), in accordance with crossover homeostasis, and both crossover and non-crossover events are more uniformly distributed. At a finer scale, recombination events overlap CpG islands more often than expected by chance, as expected in the absence of PRDM9. Estimates of the degree of GC-biased gene conversion (59%), the mean non-crossover conversion tract length (~32 bp), and the non-crossover-to-crossover ratio (5.4:1) are all comparable to those reported in primates and mice. Therefore, properties of germline mutation and recombination resolutions remain similar over large phylogenetic distances.

Reasons why chromosomal rearrangements spread to fixation and frequently distinguish related taxa remain poorly understood. We used cytological descriptions of karyotype to identify large pericentric inversions between species of Estrildid finches (family Estrildidae) and a time-dated phylogeny to assess the genomic, geographic, and phylogenetic context of karyotype evolution in this group. Inversions between finch species fixed at an average rate of one every 2.26 My. Inversions were twice as likely to fix on the sex chromosomes compared to the autosomes. A high repeat density on the sex chromosomes may increase mutation rates, but other explanations via mutagenic input are not supported, as the number of inversions on a chromosome does not correlate with its length or map size. Inversions have fixed 3.3× faster in three continental clades than in two island chain clades, and fixation rate correlates with both range size and the number of sympatric species pairs. These results point to adaptation as the dominant mechanism driving fixation and suggest a role for gene flow in karyotype divergence. A review shows that the rapid karyotype evolution observed in the Estrildid finches appears to be more general across birds, and by implication other understudied taxa.

Anthropogenic habitat loss and climate change threaten global biodiversity. Effective conservation management is greatly benefited by a detailed understanding of geographic structure, genetic diversity, and demography of threatened species. The black‐throated finch, Poephila cincta, is an Australian songbird with two subspecies: atropygialis and cincta. The southern subspecies, cincta, has experienced an ~80% range contraction over the last century and is listed as endangered, but genetic surveys of it are incomplete. Here, we use a combination of reduced representation and whole genome sequencing to examine genetic differentiation, spatial genetic structure, and demographic history in both subspecies of this species. We find that atropygialis and cincta are geographically isolated by a biogeographic barrier known as the Einasleigh Uplands and genetically distinct despite a history of divergence with gene flow. Since they last shared a common ancestor ~360,000 years ago, the two subspecies have experienced distinct demographic trajectories over the last ~100,000 years, characterized by population expansion in atropygialis and population decline in cincta. We find that the two remnant population centers of cincta, from the Galilee Basin and the Townsville Coastal Plain, each represent genetically distinct lineages that last shared appreciable levels of gene flow ~3000 years ago. Moreover, we report striking microgeographic genetic structure from the Townsville Coastal Plain between populations < 20 km apart associated with barriers to dispersal caused by anthropogenic habitat modification over the last 50 years: namely, the construction of the Ross River Dam. Our findings highlight the urgent need for a conservation approach that prioritizes habitat restoration to re‐establish population connectivity in the endangered southern black‐throated finch. The endangered southern black‐throated finch Poephila cincta cincta has experienced an ~80% range contraction over the last century, and ongoing habitat loss increases the risk of its extinction. Using reduced representation and whole genome sequencing, we examine the divergence history of northern and southern black‐throated finches and find evidence of fine‐scale genetic structure between populations of this endangered finch < 20 km apart in one remaining stronghold. Barriers to gene flow appear to be associated with anthropogenic habitat modification and hence support habitat restoration as a conservation priority.

Mating behavior can play a key role in speciation by inhibiting or facilitating gene flow between closely related taxa. Hybrid zones facilitate a direct examination of mating behavior and the traits involved in establishing species barriers. The long‐tailed finch (Poephila acuticauda) has two hybridizing subspecies that differ in bill color (red and yellow), and the yellow bill phenotype appears to have introgressed ~350 km eastward following secondary contact. To examine the role of mate choice on bill color introgression, we performed behavioral assays using natural and manipulated bill colors. We found an assortative female mating preference for males of their own subspecies when bill color was not manipulated. However, we did not find this assortative preference in trials based on artificially manipulated bill color. This could suggest that assortative preference is not fixed entirely on bill color and instead may be based on a different trait (e.g., song) or a combination of traits, or alternatively may be due to lower statistical power alongside the bill manipulations being unconvincing to the female choosers. Intriguingly, we find a bias in the inheritance of bill color in captive bred F1 hybrid females. Previous modeling suggests that assortative mate preference and this kind of partial dominance in the underlying genes may together contribute to introgression, making the genetic architecture of bill color in this system a priority for future research. We investigate whether mate choice might play a role in the unidirectional introgression of yellow bill color between subspecies of the long‐tailed finch. Females demonstrate an assortative mate preference for unmanipulated males of their own subspecies. However, the evidence that females base this assortative preference on bill color is equivocal.

Chromosomal inversions evolve frequently but the reasons for this remain unclear. We used cytological descriptions of 411 species of passerine birds to identify large pericentric inversion differences between species, based on the position of the centromere. Within 81 small clades comprising 284 of the species, we found 319 differences on the 9 largest autosomes combined, 56 on the Z chromosome, and 55 on the W chromosome. We also identified inversions present within 32 species. Using a new fossil-calibrated phylogeny, we examined the phylogenetic, demographic and genomic context in which these inversions have evolved. The number of inversion differences between closely related species is consistently predicted by whether the ranges of species overlap, even when time is controlled for as far as is possible. Fixation rates vary across the autosomes, but inversions are more likely to be fixed on the Z chromosome than the average autosome. Variable mutagenic input alone (estimated by chromosome size, map length, GC content or repeat density) cannot explain the differences between chromosomes in the number of inversions fixed. Together, these results support a model in which inversions increase because of their effects on recombination suppression in the face of hybridization. Other factors associated with hybridization may also contribute, including the possibility that inversions contain incompatibility alleles, making taxa less likely to collapse following secondary contact. Ranges of species overlap predict chromosome inversion differences between closely related passerine birds, suggesting that inversions have the selective advantage of suppressing recombination when hybridization occurs.

The exploration of hybrid zones and the intergenomic conflicts exposed through hybridization provide windows into the processes of divergence and speciation. Sex chromosomes and mitonuclear incompatibilities have strong associations with the genetics of hybrid dysfunction. In ZW sex-determining systems, maternal co-inheritance of the mitochondrial and W chromosomes immediately exposes incompatibilities between these maternal contributions of one species and the Z chromosome of another. We analyze mitochondrial and Z chromosome admixture in the long-tailed finch (Poephila acuticauda) of Australia, where hybridizing subspecies differ prominently in Z chromosome genotype and in bill color, yet the respective centers of geographic admixture for these two traits are offset by 350 km. We report two well-defined mitochondrial clades that diverged ~0.5 million years ago. Mitochondrial contact is geographically co-located within a hybrid zone of Z chromosome admixture and is displaced from bill color admixture by nearly 400 km. Consistent with Haldane’s rule expectations, hybrid zone females are significantly less likely than males to carry an admixed Z chromosome or have mismatched Z-mitochondrial genotypes. Furthermore, there are significantly fewer than expected mitonuclear mismatches in hybrid zone females and paternal backcross males. Results suggest a potential for mitonuclear/sex chromosome incompatibilities in the emergence of reproductive isolation in this system.

Background A long-standing view of Indian biodiversity is that while rich in species, there are few endemics or in-situ radiations within the subcontinent. One exception is the Western Ghats biodiversity hotspot, an isolated mountain range with many endemic species. Understanding the origins of the montane-restricted species is crucial to illuminate both taxonomic and environmental history. Results With evidence from genetic, morphometric, song, and plumage data, we show that two songbird lineages endemic to the Western Ghats montane forest each have diversified into multiple distinct species. Historically labeled as single species of widespread Asian genera, these two lineages are highly divergent and do not group with the taxa in which they were previously classified but rather are distinct early divergences in larger Asian clades of flycatchers and babblers. Here we designated two new genera, the Western Ghats shortwings as Sholicola and the laughingthrushes as Montecincla , and evaluated species-limits to reflect distinct units by revising six previously named taxa and describing one novel species. Divergence dating showed that both these montane groups split from their Himalayan relatives during the Miocene, which is coincident with a shift towards arid conditions that fragmented the previously contiguous humid forest across peninsular India and isolated these lineages in the Western Ghats. Furthermore, these two genera showed congruent patterns of diversification across the Western Ghats Sky Islands, coincident with other climatic changes. Conclusion Our study reveals the existence of two independent endemic radiations in the high montane Western Ghats or Shola Sky Islands with coincident divergence times, highlighting the role of climate in the diversification of these ancient lineages. The endemic and highly divergent nature of these previously unrecognized species underscores the dearth of knowledge about the biogeography of the Asian tropics, even for comparatively well-known groups such as birds. The substantial increase in the diversity of this region underscores the need for more rigorous systematic analysis to inform biodiversity studies and conservation efforts.

The widespread application of high-throughput sequencing in studying evolutionary processes and patterns of diversification has led to many important discoveries. However, the barriers to utilizing these technologies and interpreting the resulting data can be daunting for first-time users. We provide an overview and a brief primer of relevant methods (e.g., whole-genome sequencing, reduced-representation sequencing, sequence-capture methods, and RNA sequencing), as well as important steps in the analysis pipelines (e.g., loci clustering, variant calling, whole-genome and transcriptome assembly). We also review a number of applications in which researchers have used these technologies to address questions related to avian systems. We highlight how genomic tools are advancing research by discussing their contributions to 3 important facets of avian evolutionary history. We focus on (1) general inferences about biogeography and biogeographic history, (2) patterns of gene flow and isolation upon secondary contact and hybridization, and (3) quantifying levels of genomic divergence between closely related taxa. We find that in many cases, high-throughput sequencing data confirms previous work from traditional molecular markers, although there are examples in which genome-wide genetic markers provide a different biological interpretation. We also discuss how these new data allow researchers to address entirely novel questions, and conclude by outlining a number of intellectual and methodological challenges as the genomics era moves forward.