Painting of a quagga stallion by Nicolas Marechal, 1793. Photo from Wikipedia.
In their recent PNAS paper*, Hákon et al. generate full genome sequence data for each living species of asses and zebras, thus completing the set of genomes available for all extant species in the genus Equus (genomes for the donkey and horse have been published previously- see references below). The authors also collected full genome data for the quagga (Equus quagga quagga), a subspecies of the plains zebra that lived in South Africa until being driven to extinction in the 19th century. The last captive individual died in an Amsterdam zoo in 1883. In 1984, the quagga was the first extinct species to have its DNA sequenced. Hákon et al. used the Equus genome sequences to search for loci under selection, reconstruct demographic history, and measure gene flow among diverging lineages.
Equine phylogeny, selection scan, and karyotypic and mutational changes. (A) Inferred number of chromosome pairs for each ancestral node. (B) Phylogenetic chronogram of lineage divergence in equids based on a relaxed molecular clock. All nodes received 100% bootstrap support. The names of the genes showing evidence of positive selection are reported above the branches concerned. The numbers provided below branches refer to rates of gene loss and chromosome gains and losses, respectively. The numbers of chromosome pairs (dominant form) are indicated below species names. Figure and caption from Hakon et al. 2014.
The study showed that noncabelline (i.e. non-horse) equids formed two monophyletic groups representing the zebras and asses (see the figure above). Living equids have a wide range of chromosome pairs (from 16 in mountain zebras to 33 in Przewalski’s horse) and Hákon et al. found higher rates of chromosome loss than gain, suggesting the Equus ancestor had between 38 and 42 pairs of chromosomes.
Analysis of dN/dS ratios suggested positive selection in 48 genes with functions involved in cellular interactions, trafficking, metabolism, development, olfaction, and immunity.
Interestingly, mountain zebras showed positive selection signatures at VPS13A, a gene associated with locomotory and behavioral disorders, possibly in relation to their high sociability. The antiporter SLC9A4, involved in pH regulation and countering of adverse environmental conditions, was found to be positively selected in plains zebras, which experience a wide range of environments throughout their geographical range. Similarly, the axonal guidance factor SEMA5A, associated with cranial vascular patterning in mice and hippo- campal volume and autism in humans, was found to have undergone positive selection in the extinct quagga.
Demographic reconstructions showed that most species expanded after the Eemian about 125,000 years ago with a subsequent crash in the last 30,000 years, possibly due to climate changes in the late Pleistocene. The authors also estimated divergence times among the species.
We found that the early population split between Asiatic and African asses occurred ∼1.7 Mya. Onagers and kiang populations diverged more recently (∼266–392 kya), whereas the three populations of living zebras had already diverged ∼1.1 Mya. The extinct quagga split from the plains zebra population only ∼233–356 kya.
Finally, Hákon et al. quantified levels of gene flow among the Equus species using an approach, which tests for an excess of shared polymorphisms between one of two closely related lineages and a third lineage. Overall, the authors found evidence for four major episodes of gene flow among Equus species: 1) during the earliest Equus divergence, 2) from kiang into the donkey lineage, 3) between the Somali wild ass and Grevy’s zebra, and 4) between African asses and the mountain zebra.
[Given the evidence of gene flow among equids] we conclude that such massive karyotypic changes have not resulted in full reproductive isolation, in stark contrast with theories assuming that chromosomal impairment during meiosis is responsible for complete sterility in hybrids, but in agreement with the description of fertile offspring across equine species.
Reference:
Jónsson, Hákon, Mikkel Schubert, Andaine Seguin-Orlando, Aurélien Ginolhac, Lillian Petersen, Matteo Fumagalli, Anders Albrechtsen et al. “Speciation with gene flow in equids despite extensive chromosomal plasticity.” Proceedings of the National Academy of Sciences 111, no. 52 (2014): 18655-18660. DOI: 10.1073/pnas.1412627111
Orlando, Ludovic, Aurélien Ginolhac, Guojie Zhang, Duane Froese, Anders Albrechtsen, Mathias Stiller, Mikkel Schubert et al. “Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.”Nature 499, no. 7456 (2013): 74-78. DOI: 10.1038/nature12323
Wade, C. M., Elena Giulotto, Snaevar Sigurdsson, M. Zoli, S. Gnerre, Freyja Imsland, T. L. Lear et al. “Genome sequence, comparative analysis, and population genetics of the domestic horse.” Science 326, no. 5954 (2009): 865-867. DOI: 10.1126/science.1178158
*Thanks to Genevieve Mount for the paper suggestion!