Reproductive barriers and genomic hotspots of adaptation during allopatric species divergence: datasets for all phylogenetic reconstructions represented in Fig 2

Theory predicts that in allopatric populations, genomic divergence and
reproductive barriers may be driven by random genetic drift, and thereby
evolve slowly in large populations. However, local adaptation and
divergence under selection may also play important roles, which remain
poorly characterised. Here we address three key questions in young
allopatric species: (a) How widespread are genomic signatures of adaptive
divergence?, (b) What is the functional space along which young sister
species show divergence at the genomic level?, and (c) How quickly might
prezygotic and postzygotic reproductive barriers evolve? Analysis of 82
re-sequenced genomes of the Oriental Papilio polytes species group
revealed surprisingly widespread hotspots of intense selection and
selective sweeps at hundreds of genes, and spanning all chromosomes,
rather than divergence only in a few genomic islands. These genes are
involved in diverse ecologically important adaptive functions such as wing
development, colour patterning, courtship behaviour, mimicry, pheromone
synthesis and olfaction, and host plant use and digestion of secondary
metabolites, that could contribute to local adaptation and subsequent
reproductive isolation. Divergence at such functional genes appeared to
have evolved in conjunction with reproductive consequences: behavioural
and hybridisation experiments revealed strong assortative mate preference
(prezygotic barriers) as well as postzygotic barriers to hybridisation in
timespans as short as 1.5 my, indicating that speciation was already
complete, rather than incipient. Our study thus demonstrates an
underappreciated role of intense selection and potential local adaptation
in creating genome-wide hotspots of rapid molecular evolution and
divergence, during differentiation and speciation in young allopatric
species.