SignificanceIt is a tenet of modern biology that species adapt through natural selection to cope with the ever-changing environment. By comparing genetic variants between the island and mainland populations of a passerine, we inferred the related age of genetic variants across its entire genome and suggest that preexisting standing variants played the predominant role in local adaptation. Our findings not only resolve a long-standing fundamental problem in biology regarding the genetic sources of adaptation, but imply that the evolutionary potential of a population is highly associated with its preexisting genetic variation.
Allopatry is conventionally considered the geographical mode of speciation for continental island organisms. However, strictly allopatric speciation models that assume the lack of postdivergence gene flow seem oversimplified given the recurrence of land bridges during glacial periods since the late Pliocene. Here, to evaluate whether a continental island endemic, the Taiwan hwamei (Leucodioptron taewanus, Passeriformes Timaliidae) speciated in strict allopatry, we used weighted-regression-based approximate Bayesian computation (ABC) to analyse the genetic polymorphism of 18 neutral nuclear loci (total length: 8500 bp) in Taiwan hwamei and its continental sister species, the Chinese hwamei (L. canorum canorum). The nonallopatry model was found to fit better with observed genetic polymorphism of the two hwamei species (posterior possibility = 0.82). We also recovered unambiguous signals of nontrivial bidirectional postdivergence gene flow (N(e)m >> 1) between Chinese hwamei and Taiwan hwamei until 0.5 Ma. Divergence time was estimated to be 3.5 to 2 million years earlier than that estimated from mitochondrial cytochrome b sequences. Finally, using the inferred nonallopatry model to simulate genetic variation at 24 nuclear genes examined showed that the adiponectin receptor 1 gene may be under divergent adaptation. Our findings imply that the role of geographical barrier may be less prominent for the speciation of continental island endemics, and suggest a shift in speciation studies from simply correlating geographical barrier and genetic divergence to examining factors that facilitate and maintain divergence, e.g. differential selection and sexual selection, especially in the face of interpopulation gene flow.
Due to the male's elaborate songs, the Hwamei Garrulax canorus is the most popular caged bird in the global Chinese community. Three allopatric Hwamei subspecies have been described: G. c. canorus in central and southern China and northern Indochina, G. c. owstoni from Hainan and G. c. taewanus from Taiwan. We sequenced the entire mitochondrial cytochrome b gene to reconstruct the molecular intraspecific phylogeny of the Hwamei. Molecular phylogenetic trees indicated that individuals of the three subspecies formed three monophyletic clades with high bootstrap support (> 95%). The basal clade was G. c. taewanus. According to a conventional molecular clock (2% divergence per million years), G. c. taewanus split from the other Hwamei taxa around 1.5 million years ago, and G. c. owstoni diverged from G. c. canorus around 0.6 million years ago. Considering the periodic connection between the Asian mainland and nearby continental islands during the glacial periods, habitat vicariance may have played a more important role than geographical vicariance in facilitating the differentiation of these taxa. Molecular diagnosability, population integrity, and concordance between the population ranges and the topology of the phylogenetic tree suggested that the Hwamei should be delimited into at least two full species: G. canorus and G. taewanus. Our work represents one of the first attempts to re‐evaluate the intraspecific systematics for an eastern Asian bird species using molecular data.
Highlights d A cortex/medulla composite beam organization allows rachides to adapt flexibly d Polarized adhesion and keratin expression lead to hooklet barbules that form vanes d With-dermal papilla WNT signaling controls barbule shape along the feather P-D axis d 3D feathers embedded in amber show primitive vanes formed by overlapping barbules
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