Phylogenomics of an extra-Antarctic notothenioid radiation reveals a previously unrecognized lineage and diffuse species boundaries

SANTIAGO GUILLERMO CEBALLOS; MARIUS ROESTI; MICHAEL MATSCHINER; DANIEL ALFREDO FERNANDEZ; MALTE DAMERAU; REINHOLD HANEL; WALTER SALZBURGER

BMC EVOLUTIONARY BIOLOGY

BIOMED CENTRAL LTD

Lugar: Londres; Año: 2019

1471-2148

BackgroundThe impressive adaptive radiation of notothenioid fishes in Antarctic waters is generallythought to have been facilitated by an evolutionary key innovation, antifreezeglycoproteins, permitting the rapid evolution of more than 120 species subsequent tothe Antarctic glaciation. By way of contrast, the second-most species-rich notothenioidgenus, Patagonotothen, which is nested within the Antarctic clade of Notothenioidei, isalmost exclusively found in the non-Antarctic waters of Patagonia. While the drivers ofthe diversification of Patagonotothen are currently unknown, they are unlikely to berelated to antifreeze glycoproteins, given that water temperatures in Patagonia are wellabove freezing point. Here we performed a phylogenetic analysis based on genomewidesingle nucleotide polymorphisms (SNPs) derived from restriction site-associatedDNA sequencing (RADseq) in a total of twelve Patagonotothen species.ResultsWe present a well-supported, time-calibrated phylogenetic hypothesis including closelyand distantly related outgroups, confirming the monophyly of the genusPatagonotothen with an origin approximately 3 million year ago and the paraphyly ofboth the sister genus Lepidonotothen and the family Notothenidae. Our phylogenomicand population genetic analyses highlight a previously unrecognized linage andprovide evidence for shared genetic variation between some closely related species.We also provide a mitochondrial phylogeny showing mitonuclear discordance.ConclusionsBased on a combination of phylogenomic and population genomic approaches, weprovide evidence for the existence of a new, potentially cryptic, Patagonotothenspecies, and demonstrate that genetic boundaries between some closely relatedspecies are diffuse, likely due to recent introgression and/or incomplete linage sorting.The detected mitonuclear discordance highlights the limitations of relying on a singlelocus for species barcoding. In addition, our time calibrated phylogenetic hypothesisshows that the early burst of diversification roughly coincides with the onset of theintensification of Quaternary glacial cycles and that the rate of species accumulationmay have been stepwise rather than constant. Our phylogenetic framework not onlyadvances our understanding of the origin of a high-latitude marine radiation, but alsoprovides the basis for the study of the ecology and life history of the genusPatagonotothen, as well as for their conservation and commercial management.