Parallel evolution in an island archipelago revealed by genomic sequencing of Hipposideros leaf-nosed bats.

Body size is a key morphological attribute, often used to delimit species boundaries among closely related taxa. But body size can evolve in parallel, reaching similar final states despite independent evolutionary and geographic origins, leading to faulty assumptions of evolutionary history. Here, we document parallel evolution in body size in the widely distributed leaf-nosed bat genus Hipposideros, which has misled both taxonomic and evolutionary inference. We sequenced reduced representation genomic loci and measured external morphological characters from three closely related species from the Solomon Islands archipelago, delimited by body size. Species tree reconstruction confirms the paraphyly of two morphologically designated species. The nonsister relationship between large-bodied H. dinops lineages found on different islands indicates that large-bodied ecomorphs have evolved independently at least twice in the history of this radiation. A lack of evidence for gene flow between sympatric, closely related taxa suggests the rapid evolution of strong reproductive isolating barriers between morphologically distinct populations. Our results position Solomon Islands Hipposideros as a novel vertebrate system for studying the repeatability of parallel evolution under natural conditions. We conclude by offering testable hypotheses for how geography and ecology could be mediating the repeated evolution of large-bodied Hipposideros lineages in the Solomon Islands.

Range-wide phylogenomics of the Great Horned Owl (Bubo virginianus) reveals deep north-south divergence in northern Peru.

The Great Horned Owl (Bubo virginianus) inhabits myriad habitats throughout the Americas and shows complex patterns of individual and geographic morphological variation. The owl family Strigidae is known to follow ecogeographic rules, such as Gloger's rule. Although untested at the species level, these ecogeographic rules may affect B. virginianus plumage coloration and body size. Previous studies have indicated that, despite this species' morphological variability, little genetic differentiation exists across parts of their range. This study uses reduced representation genome-wide nuclear and complete mitochondrial DNA sequence data to assess range-wide relationships among B. virginianus populations and the disputed species status of B. v. magellanicus (Magellanic or Lesser Horned Owl) of the central and southern Andes. We found shallow phylogenetic relationships generally structured latitudinally to the north of the central Andes, and a deep divergence between a southern and northern clade close to the Marañón Valley in the central Andes, a common biogeographic barrier. We identify evidence of gene flow between B. v. magellanicus and other subspecies based on mitonuclear discordance and F-branch statistics. Overall differences in morphology, plumage coloration, voice, and genomic divergence support species status for B. v. magellanicus.

A complete species-level phylogeny of the Erythrura parrotfinches (Aves: Estrildidae).

Identifying species boundaries and phylogenetic relationships among groups of closely related species provides a necessary framework for understanding how biodiversity evolves in natural systems. Here we present a complete phylogeny of the avian genus Erythrura (family Estrildidae) commonly known as parrotfinches, which includes species threatened by habitat loss and the pet trade. Using both mitogenome and reduced-representation genome-wide nuclear DNA sequence data, we reconstructed the evolutionary history of the group by sampling all 12 recognized species, four of which had not previously been studied in a phylogenetic context. We included intra-species geographic sampling that allowed us to comment on species limits in some taxa. We recovered the Gouldian Finch (Chloebia gouldiae) of Australia which has often been placed in the monotypic genus Chloebia, as being sister to a clade comprising all Erythrura species. In addition, we recovered a well-supported clade comprising eight species distributed throughout the Pacific Island eco-region, whereas those species occurring in continental southeast Asia, the Greater Sundas, and the Philippines, were recovered as earlier branching lineages. Of note was the early branching of the Fiji-endemic E. kleinschmidti which corroborates its unique phenotype. We also found a deep phylogenetic split (8.59% corrected, 7.89% uncorrected divergence in the mitochondrial gene ND2) between the Java and Philippine populations of E. hyperythra, indicating unrecognized species-level diversity within this taxon. In contrast, genome-wide nuclear data suggested that the New Guinea endemic species E. papuana is embedded within the widespread species E. trichroa in all phylogenetic reconstructions, corroborating previously published mitochondrial data that suggested a similar pattern. By generating a phylogenetic hypothesis for the relationships among all species of Erythrura parrotfinches, we provide a framework for better understanding the extant diversity and evolutionary history of this group.

Mitonuclear discordance results from incomplete lineage sorting, with no detectable evidence for gene flow, in a rapid radiation of Todiramphus kingfishers.

Many organisms possess multiple discrete genomes (i.e. nuclear and organellar), which are inherited separately and may have unique and even conflicting evolutionary histories. Phylogenetic reconstructions from these discrete genomes can yield different patterns of relatedness, a phenomenon known as cytonuclear discordance. In many animals, mitonuclear discordance (i.e. discordant evolutionary histories between the nuclear and mitochondrial genomes) has been widely documented, but its causes are often considered idiosyncratic and inscrutable. We show that a case of mitonuclear discordance in Todiramphus kingfishers can be explained by extensive genome-wide incomplete lineage sorting (ILS), likely a result of the explosive diversification history of this genus. For these kingfishers, quartet frequencies reveal that the nuclear genome is dominated by discordant topologies, with none of the internal branches in our consensus nuclear tree recovered in >50% of genome-wide gene trees. Meanwhile, a lack of inter-species shared ancestry, non-significant pairwise tests for gene flow, and little evidence for meaningful migration edges between species, leads to the conclusion that gene flow cannot explain the mitonuclear discordance we observe. This lack of evidence for gene flow combined with evidence for extensive genome-wide gene tree discordance, a hallmark of ILS, leads us to conclude that the mitonuclear discordance we observe likely results from ILS, specifically deep coalescence of the mitochondrial genome. Based on this case study, we hypothesize that similar demographic histories in other 'great speciator' taxa across the Indo-Pacific likely predispose these groups to high levels of ILS and high likelihoods of mitonuclear discordance.

Mismatch-induced growth reductions in a clade of Arctic-breeding shorebirds are rarely mitigated by increasing temperatures.

In seasonal environments subject to climate change, organisms typically show phenological changes. As these changes are usually stronger in organisms at lower trophic levels than those at higher trophic levels, mismatches between consumers and their prey may occur during the consumers' reproduction period. While in some species a trophic mismatch induces reductions in offspring growth, this is not always the case. This variation may be caused by the relative strength of the mismatch, or by mitigating factors like increased temperature-reducing energetic costs. We investigated the response of chick growth rate to arthropod abundance and temperature for six populations of ecologically similar shorebirds breeding in the Arctic and sub-Arctic (four subspecies of Red Knot Calidris canutus, Great Knot C. tenuirostris and Surfbird C. virgata). In general, chicks experienced growth benefits (measured as a condition index) when hatching before the seasonal peak in arthropod abundance, and growth reductions when hatching after the peak. The moment in the season at which growth reductions occurred varied between populations, likely depending on whether food was limiting growth before or after the peak. Higher temperatures led to faster growth on average, but could only compensate for increasing trophic mismatch for the population experiencing the coldest conditions. We did not find changes in the timing of peaks in arthropod availability across the study years, possibly because our series of observations was relatively short; timing of hatching displayed no change over the years either. Our results suggest that a trend in trophic mismatches may not yet be evident; however, we show Arctic-breeding shorebirds to be vulnerable to this phenomenon and vulnerability to depend on seasonal prey dynamics.

Population connectivity across a highly fragmented distribution: Phylogeography of the Chalcophaps doves.

Chalcophaps is a morphologically conserved genus of ground-walking doves distributed from India to mainland China, south to Australia, and across the western Pacific to Vanuatu. Here, we reconstruct the evolutionary history of this genus using DNA sequence data from two nuclear genes and one mitochondrial gene, sampled from throughout the geographic range of Chalcophaps. We find support for three major evolutionary lineages in our phylogenetic reconstruction, each corresponding to the three currently recognized Chalcophaps species. Despite this general concordance, we identify discordant mitochondrial and nuclear ancestries in the subspecies C. longirostris timorensis, raising further questions about the evolutionary history of this Timor endemic population. Within each of the three species, we find evidence for isolation by distance or hierarchical population structure, indicating an important role for geography in the diversification of this genus. Despite being distributed broadly across a highly fragmented geographic region known as a hotspot for avian diversification, the Chalcophaps doves show modest levels of phenotypic and genetic diversity, a pattern potentially explained by strong population connectivity owing to high overwater dispersal capability.

Inter- and intra-archipelago dynamics of population structure and gene flow in a Polynesian bird.

Islands are separated by natural barriers that prevent gene flow between terrestrial populations and promote allopatric diversification. Birds in the South Pacific are an excellent model to explore the interplay between isolation and gene flow due to the region's numerous archipelagos and well-characterized avian communities. The wattled honeyeater complex (Foulehaio spp.) comprises three allopatric species that are widespread and common across Fiji, Tonga, Samoa, and Wallis and Futuna. Here, we explored patterns of diversification within and among these lineages using genomic and morphometric data. We found support for three clades of Foulehaio corresponding to three recognized species. Within F. carunculatus, population genetic analyses identified nine major lineages, most of which were composed of sub-lineages that aligned nearly perfectly to individual island populations. Despite genetic structure and great geographic distance between populations, we found low levels of gene flow between populations in adjacent archipelagos. Additionally, body size of F. carunculatus varied randomly with respect to evolutionary history (as Ernst Mayr predicted), but correlated negatively with island size, consistent with the island rule. Our findings support a hypothesis that widespread taxa can show population structure between immediately adjacent islands, and likely represent many independent lineages loosely connected by gene flow.

Avian influenza virus antibodies in Pacific Coast Red Knots (Calidris canutus roselaari).

Prevalence of avian influenza virus (AIV) antibodies in the western Atlantic subspecies of Red Knot (Calidris canutus rufa) is among the highest for any shorebird. To assess whether the frequency of detection of AIV antibodies is high for the species in general or restricted only to C. c. rufa, we sampled the northeastern Pacific Coast subspecies of Red Knot (Calidris canutus roselaari) breeding in northwestern Alaska. Antibodies were detected in 90% of adults and none of the chicks sampled. Viral shedding was not detected in adults or chicks. These results suggest a predisposition of Red Knots to AIV infection. High antibody titers to subtypes H3 and H4 were detected, whereas low to intermediate antibody levels were found for subtypes H10 and H11. These four subtypes have previously been detected in shorebirds at Delaware Bay (at the border of New Jersey and Delaware) and in waterfowl along the Pacific Coast of North America.