Abstract
Colossendeis megalonyx Hoek, 1881 has the broadest distribution of all sea spiders in the Southern Ocean. Previous studies have detected several evolutionarily young lineages within this taxon and interpreted them as a result of allopatric speciation in a few shelf refuges during glacial maxima. However, alternative scenarios such as ecological speciation in sympatry have rarely been considered or tested. Here, we generated the most extensive genomic and morphometric data set on the C. megalonyx species complex to (i) comprehensively describe species diversity, (ii) explore intraspecific connectivity between populations located around Antarctica, and (iii) systematically test for positive selection indicative of adaptive speciation. We successfully applied a target hybrid enrichment approach and recovered all 1607 genes targeted. Phylogenomic analysis was consistent with previous findings and, moreover, increased the resolution of branching within lineages. We found specimens of phylogenetically well-separated lineages occurring in sympatry to be genetically distinct from each other and gene flow between geographically separated populations of the same lineages to be restricted. Evidence for positive selection was found for four genes associated with structural and neuronal functions. Hence, there is an indication for positive selection in the C. megalonyx species complex, yet its specific contribution to the speciation process remains to be explored further. Finally, morphometric analyses revealed multiple significant differences between lineages, but a clear separation proved difficult. Our study highlights the relevance of positive selection as a potential driver for speciation in the Southern Ocean.
Highlights
The Southern Ocean accommodates a unique, speciose and highly endemic benthic community (Knox and Lowry 1977; Clarke and Johnston 2003; Aronson et al 2007; Clarke 2008) that has evolved through in situ radiations after the1 3 Vol.:(0123456789)Polar Biology (2020) 43:319–342 opening of the Drake Passage and the subsequent establishment of the Polar Front
Sequencing of target hybrid enrichment libraries of specimens of the Colossendeis megalonyx species complex resulted in an average number of 426,047 reads per individual (standard deviation (SD) 67,634)
99.6% of the 1607 targeted genes were recovered per individual for the Colossendeis megalonyx species complex using hybrid enrichment
Summary
The Southern Ocean accommodates a unique, speciose and highly endemic benthic community (Knox and Lowry 1977; Clarke and Johnston 2003; Aronson et al 2007; Clarke 2008) that has evolved through in situ radiations after the1 3 Vol.:(0123456789)Polar Biology (2020) 43:319–342 opening of the Drake Passage (about 30 mya) and the subsequent establishment of the Polar Front (see Poulin et al 2002; Briggs 2003; Convey et al 2009). Prominent examples of early in situ radiations during the Mio- and Pliocene include the Antarctic icefishes (Notothenioidei, Eastman and McCune 2000), octopuses (Strugnell et al 2012), and serolid isopods (Brandt 1991; Held 2000). In addition to these ancient radiations, molecular studies revealed a high number of recent divergences that probably occurred in the Plio- and Pleistocene (e.g., Convey et al 2009; Fraser et al 2012; Halanych and Mahon 2018 for overviews). The often allopatric occurrence of cryptic species adds strong support for this hypothesis (e.g., Held 2003; Held and Wägele 2005; Wilson et al 2007)
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