Genomic signatures of isolation, hybridization, and selection during speciation of island finches

Sister species occurring sympatrically on islands are rare and offer unique opportunities to understand how speciation can proceed in the face of gene flow. The São Tomé grosbeak is a massive-billed, 'giant' finch endemic to the island of São Tomé in the Gulf of Guinea, where it has diverged from its co-occurring sister species the Príncipe seedeater, an average-sized finch that also inhabits two neighbouring islands. Here, we show that the grosbeak carries a large number of unique alleles different from all three Príncipe seedeater populations, but also shares many alleles with the sympatric São Tomé population of the seedeater, a genomic signature signifying divergence in isolation as well as subsequent introgressive hybridization. Furthermore, genomic segments that remain unique to the grosbeak are situated close to genes, including genes that determine bill morphology, suggesting the preservation of adaptive variation through natural selection during divergence with gene flow. This study reveals a complex speciation process whereby genetic drift, introgression, and selection during periods of isolation and secondary contact all have shaped the diverging genomes of these sympatric island endemic finches.

Nesting Success and Nesting Height in the Critically Endangered Medium Tree Finch (Camarhynchus pauper)

When different introduced species across trophic levels (parasite, predator) invade island systems, they may pose significant threats to nesting birds. In this study, we measure nesting height and infer causes of offspring mortality in the critically endangered Medium Tree Finch (Camarhynchus pauper), an island endemic restricted to Floreana Island on the Galápagos Archipelago. Considering all nests at which a male built a nest, sang and attempted to attract a female (n = 222 nests), only 10.4% of nests produced fledglings (5% of nests had total fledging success, 5.4% of nests had partial fledging success). Of the 123 nests chosen by a female, 18.7% produced fledglings and of 337 eggs laid, 13.4% produced fledglings. Pairing success was higher for older males, but male age did not predict nesting success. All nests with chicks were infested with avian vampire fly larvae (Philornis downsi). We attributed the cause of death to avian vampire fly if chicks were found dead in the nest with fly larvae or pupae (45%) present. We inferred avian (either Asio flammeus galapagoensis or Crotophaga ani) predation (24%) if the nest was empty but dishevelled; and black rat (Rattus rattus) predation (20%) if the nest was empty but undamaged. According to these criteria, the highest nests were depredated by avian predators, the lowest nests by rats, and intermediate nests failed because of avian vampire fly larvae. In conclusion, there is no safe nesting height on Floreana Island under current conditions of threats from two trophic levels (introduced parasitic dipteran, introduced mammalian/avian predators; with Galápagos Short-Eared Owls being the only native predator in the system).

Eradication of a highly invasive bird, the Common Myna Acridotheres tristis, facilitates the establishment of insurance populations of island endemic birds

Summary Common Myna Acridotheres tristis is considered to be among the world’s most damaging invasive species through disturbance, predation, competition pathogen introduction to native birds and other taxa. Claimed impacts on native birds have often been based on anecdotal reports. More substantive evidence of interference with small-island endemic birds has been reported, but impacts have rarely been quantified or subjected to experimental manipulation. On Denis Island (Seychelles), up to 10% of Seychelles Warblers Acrocephalus sechellensis, and small numbers of Seychelles Fodies Foudia sechellesis and Seychelles Paradise Flycatchers Terpsiphone corvina had head injuries following myna attacks, stimulating an eradication of the mynas. Populations of four species of Seychelles’ endemic birds, introduced to the island to establish insurance populations, were estimated before, during and after the completion of the eradication, permitting assessment of the impact of myna removal on populations of the endemics. Numbers of all four endemics increased following introduction, but increases in the numbers of Seychelles Magpie Robins Copsychus sechellensis and Seychelles Paradise Flycatchers accelerated after >90% of the mynas had been removed. All endemic populations continued to increase during and after completion of the eradication in 2015, and injuries to Seychelles Warblers, Seychelles Fodies, and Seychelles Paradise Flycatchers ceased. Habitat management within a designated conservation zone on the island, into which the endemics were released and subsequently spread to occupy most of the island, also contributed to the endemic birds’ global populations and to their improved conservation status. This study confirms that mynas negatively impact small island populations of endemic birds and suggests that their potential impact has been underestimated. Myna eradication should be considered vital before endangered endemic birds and other taxa susceptible to their negative impacts are translocated to small islands for conservation reasons.

Challenges of applying monophyly in the phylogenetic shallows: taxonomic reappraisal of the Dactylorhiza maculata group

SummaryThe first study of the taxonomically critical European orchid genus Dactylorhiza to use next-generation DNA sequencing generated the statistically best-supported reconstruction of its phylogeny to date. However, the two competing topologies obtained within the monophyletic Section Maculatae differed radically in the placement of the D. maculata s.s.–D. foliosa clade. Both topologies showed D. foliosa to be nested deeply within D. maculata s.s., and suggested that D. saccifera s.l. is paraphyletic, D. saccifera s.s. from south-eastern Europe and Asia Minor diverging before D. gervasiana from south-central Europe (a taxon typically viewed as a subspecies of D. saccifera or, more often, ignored completely). The poorly-sampled but character-rich morphometric comparison presented here suggests that D. saccifera s.s. and D. gervasiana cannot be distinguished with confidence using morphological characters and that, if D. gervasiana is accepted as a species, it is effectively cryptic. The diploid D. foliosa is accepted as an island endemic species, despite rendering paraphyletic the autotetraploid D. maculata s.s.; all other named taxa within the D. maculata s.s. clade are considered infraspecific. Dactylorhiza fuchsii is indisputably a bona fide species rather than a subspecies but it does not merit becoming the basis of a taxonomic section separate from D. maculata s.s. The strongly contrasting degrees of molecular vs morphological disparity reported here are representative of a more general trend evident in groups that have experienced comparatively recent speciation, as is the need to recognise occasional paraphyletic species when circumscribing species by integrating genotypic and phenotypic data categories. Explicit taxonomic criteria combined with a comparative, monographic approach are needed to achieve consistency of ranking. Disproving hypotheses of species status is judged a criminally underrated activity, actually being as important to outcomes as much-vaunted species "discovery".

Low diversity, little genetic structure but no inbreeding in a high density island endemic pit-viper Gloydius shedaoensis

Islands species and their ecosystems play an important role in global biodiversity preservation, and many vulnerable island species are conservation priorities. Although insular habitat likely facilitates the species diversification process, it may also aggravate the fragility of these species with high risk of inbreeding. The Shedao pit-viper Gloydius shedaoensis is an island endemic species with an extremely high population density, which has been categorized as vulnerable in the IUCN Red List. We collected 13,148 SNP from across its genome and examined its genetic diversity and demographic history. The Shedao pit-viper has a low genetic diversity but shows no sign of inbreeding. Furthermore, population genetic structure analysis, including the NJ tree, PCoA, clustering, and spatial autocorrelation, revealed a general lack of spatial structure. Only the IBD residues suggested a weak patchiness. Overall, the population is nearly panmictic and gene flow is evenly distributed across the island. The large number of individuals, small size of the island, and the lack of population structure likely all contribute to the lack of inbreeding in this species. We also detected signs of male-biased dispersal, which likely is another inbreeding avoidance strategy. Historical demographic analysis suggested that the historical population size and distribution of the species are much larger than their current ones. The multiple transgressive-regressive events since the Late Pleistocene are likely the main cause of the population size changes. Taken together, our results provide a basic scientific foundation for the conservation of this interesting and important species.

Drosophila sechellia: A Genetic Model for Behavioral Evolution and Neuroecology

Defining the mechanisms by which animals adapt to their ecological niche is an important problem bridging evolution, genetics, and neurobiology. We review the establishment of a powerful genetic model for comparative behavioral analysis and neuroecology, Drosophila sechellia. This island-endemic fly species is closely related to several cosmopolitan generalists, including Drosophila melanogaster, but has evolved extreme specialism, feeding and reproducing exclusively on the noni fruit of the tropical shrub Morinda citrifolia. We first describe the development and use of genetic approaches to facilitate genotype/phenotype associations in these drosophilids. Next, we survey the behavioral, physiological, and morphological adaptations of D. sechellia throughout its life cycle and outline our current understanding of the genetic and cellular basis of these traits. Finally, we discuss the principles this knowledge begins to establish in the context of host specialization, speciation, and the neurobiology of behavioral evolution and consider open questions and challenges in the field. Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.