Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus

Abstract

Background: Elucidating the process of speciation requires an in-depth understanding of the evolutionary history of the species in question. Studies that rely upon a limited number of genetic loci do not always reveal actual evolutionary history, and often confuse inferences related to phylogeny and speciation. Whole-genome data, however, can overcome this issue by providing a nearly unbiased window into the patterns and processes of speciation. In order to reveal the complexity of the speciation process, we sequenced and analyzed the genomes of 10 wild pigs, representing morphologically or geographically well-defined species and subspecies of the genus Sus from insular and mainland Southeast Asia, and one African common warthog.

Results: Our data highlight the importance of past cyclical climatic fluctuations in facilitating the dispersal and isolation of populations, thus leading to the diversification of suids in one of the most species-rich regions of the world. Moreover, admixture analyses revealed extensive, intra- and inter-specific gene-flow that explains previous conflicting results obtained from a limited number of loci. We show that these multiple episodes of gene-flow resulted from both natural and human-mediated dispersal.

Conclusions: Our results demonstrate the importance of past climatic fluctuations and human mediated translocations in driving and complicating the process of speciation in island Southeast Asia. This case study demonstrates that genomics is a powerful tool to decipher the evolutionary history of a genus, and reveals the complexity of the process of speciation.

Figure 1

Geographic distribution, phylogenetic relationships and admixture between Sus lineages. (A) A map of Island and Mainland Southeast Asia depicting the modern distributions of five Sus species. The grey shaded area represents the maximum geographical extent of Sundaland during periods of low sea level. (B) Phylogenetic relationships among Sus species inferred from nuclear DNA. Node labels show age in millions of years and 95% confidence interval. Grey shading highlights taxa living on Sundaland (C,D) Diagrams depicting the excess derived allele sharing when comparing sister taxa and outgroups. Each row contains the fraction of excess allele sharing by a taxon (left/right) with the top label/outgroup (S. scrofa or S. barbatus) relative to its sister taxon (left/right). The grey bar points in the direction of the taxon that shares more derived alleles with the outgroup than its sister taxon, and its magnitude indicates the amount of excess (D). Black bars represent 1 standard error and stars indicate D values significantly different from 0 (P < 0.01; see Materials and methods). (E) A mitochondrial DNA Bayesian phylogenetic-based tree with node labels that represent posterior probabilities (* > 0.85; ** = 1).

Figure 2

A eustatic curve adapted from [18]. (A) Each black bar shows 95% confidence interval of each divergence event as inferred from molecular clock analysis (Figure 1B). (B) Eustatic curve for the last 5 My. (C) Legend of events represented as black bars in (A).

Figure 3

Population sizes of Sus in ISEA inferred from autosomes. Sumatra1/2 = S. scrofa population from Sumatra. S.verru = S. verrucosus; S.cele = S. celebensis; S.cebi = S. cebifrons; S.barba = S. barbatus.