It would seem that between the global hitchhiking of feral pigs with human migration, America’s absurd obsession with bacon and the possible emergence of pandemic influenza via recombination of human and porcine strains, the past, present and future of our civilization are inextricably linked to that of the domestic pig. With that in mind, let’s have a look at a recent paper on the evolutionary history of the genus Sus by Frantz et al. 2013.
Domestic pigs are in the family Suidae, which includes the babirusas, warthogs, the endangered pygmy hog (whose generic name is, Porcula, seems a likely candidate for America’s next tragic children’s cereal) and the domestic pig’s close relatives in the genus Sus. Depending on where you draw the lines, there are around 7 species in Sus. With the exception of the wild boar (Sus scrofa) their natural ranges are restricted to Southeast Asia west of Wallace’s Line. Extant species of Sus have diversified recently (sharing a common ancestor ~5 million years ago) and the species are all thought capable of producing viable hybrid offspring. Most species are restricted to single islands or island complexes in Southeast Asia (such as Borneo, Java and the Philippines). Previous phylogenetic estimates of the genus are in conflict over the relationships among species.
The wild boar is naturally occurring in much of Eurasia and consists of a number of deeply divergent populations. It is the progenitor of the domestic pig, and thought to have been domesticated on at least two occasions, once in the Middle East and once in China. More domestications have been suggested based on mtDNA phylogeography (e.g. Larson et al. 2005), but given the possibility of introgressive hybridization between domestic and wild populations, the evidence seems equivocal to this blogger. Both domestic pigs and wild boar have been spread around the world by humans. In some cases, domestic pigs have escaped and established feral populations. Some of these populations are quite old, such that their provenance was the subject of debate (Larson et al. 2007), extremely charismatic, or have exchanged genes with either other Sus species or introduced wild boar. Introduced and feral populations of Sus scrofa can be quite destructive to natural ecosystems, but have proved nearly impossible to eradicate because of its intelligence, ecological flexibility, and perhaps most importantly, high reproductive rate.
So, problems of human introduction, propensity for hybridization, and a recent divergence history may all have prevented a clearer understanding of the evolutionary history of Sus. It is against this backdrop that Frantz et al. sequenced the complete genomes of 9 Sus individuals from five species in Eurasia. Their aim was to resolve the phylogeny and divergence times in the genus and to infer the extent of admixture between species.
They take several approaches to estimating phylogeny, including a concatenated supermatrix, a multispecies coalescent analysis and a whole mitochondrial genomic analysis. To estimate divergence times they use a fixed phylogeny, a set of fossil calibrations and restrict the data used to the subset of genomic regions that did not conflict with that phylogeny. They also assess admixture using D-statistics (I prefer the more memorable name “ABBA/BABA test”).
The authors imply that their concatenated and coalescent analyses were in agreement (the paper is in early view and the supplemental material is not available). Sus scrofa diverged earliest at 4-4.5 million years ago, and the island species all diverge between 3 and 1.5 million years ago. In parallel, subpopulations of Sus scrofa on the mainland diverged, and a single population colonized the island of Sumatra (Figure 1B, below). They infer that climate and sea level fluctuations throughout this period facilitated the dispersal and subsequent diversification of Sus across the islands of Southeast Asia.
Their mitochondrial genome phylogeny (consistent with prior analyses, Figure 1E) tells a drastically different story, with species from Borneo and Java and the Sumatran population of S. scrofa all sharing closely related haplotypes. They attribute this to widespread mitochondrial introgression in the late pleistocene (a story close to my heart) coinciding with periods of low sea level that would have united these islands into a single land mass. Supporting this argument, the ABBA-BABA tests also indicate substantial introgression of nuclear genes between these three taxa (Figures 1C/D, but see the paper for details on interpretation). Other analyses indicate admixture between the Sulawesi species S. celebensis and Sumatran S. scrofa, a likely result of human translocation, and between European S. scrofa and Southeast Asian island species, something only likely to have happened in the last few hundred years.
I think this is a pretty cool paper with a nice set of analyses. It really highlights that genomic data have a lot of power to address questions many molecular phylogenetic papers have been forced to leave unresolved over the last couple decades. Nevertheless, it also highlights a couple of the major problems that remain with this kind of data. First, like many others, the authors here used pretty ad hoc data filtering and aggregation schemes to before fitting their data to models. For example, they used only data that matched their optimal species tree to estimate divergence times. They assert that the bias from this will be toward younger divergence times and that it will be small, but I don’t think either of these is necessarily the case. Either way, we have no simulations or empirical data to resolve the issue. Second, throughout my time in grad school it was pretty exciting to see a steady march of increasingly sophisticated analytical models released, so now it’s kind of sad to see many of them tossed aside as computationally intractable in favor of summary statistics. I am by no means criticizing the authors of this paper as computational tractability is a real issue and ABBA-BABA tests are clearly pretty clever, but I’m just sayin’…
At any rate, interesting paper. Time for some bacon. I wonder what Sus barbatus tastes like…
Frantz, Laurent AF, et al. “Genome sequencing reveals fine scale diversification and reticulation history during speciation in Sus.” Genome Biology 14.9 (2013): R107.
Larson, Greger, et al. “Worldwide phylogeography of wild boar reveals multiple centers of pig domestication.” Science 307.5715 (2005): 1618-1621.
Larson, Greger, et al. “Phylogeny and ancient DNA of Sus provides insights into neolithic expansion in Island Southeast Asia and Oceania.” Proceedings of the National Academy of Sciences 104.12 (2007): 4834-4839.