Analyzing drivers of speciation in the Southern Ocean using the sea spider species complex Colossendeis megalonyx as a test case

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.

New findings and two new species of the genus Colossendeis Jarzynsky, 1870 (Pycnogonida, Colossendeidae), with a morphometric analysis for species from the Southern Ocean

“…In addition, molecular studies have revealed several cryptic lineages within the C. meglonyx complex, supporting the hypothesis that there are several unrecognized species within C. megalonyx (Krabbe et al 2010;Dietz et al 2013Dietz et al , 2015bDietz et al , 2019Dömel et al 2020). Only C. scoresbii has been confirmed to be separated from C. megalonyx (Krabbe et al 2010;Dietz et al 2019).…”

“…Only C. scoresbii has been confirmed to be separated from C. megalonyx (Krabbe et al 2010;Dietz et al 2019). More recently, a combined molecular and morphological study has revealed a high morphological variation within the clades, hindering the possible differentiation of lineages in this C. megalonyx species complex (Dömel et al 2020). Unfortunately, these clades have not been morphologically characterized and consequently have not been assigned to any Colossendeis binomen.…”

“…In the last decade, molecular analyses have been carried out on this C. megalonyx complex and a variable number of cryptic clades have been proposed (Krabbe et al 2010;Dietz et al 2015bDietz et al , 2019Dömel et al 2020). However no diagnostic morphological characters have been provided for these proposed clades, and they have not been assigned to any known species or subspecies name.…”

Sea spiders (Arthropoda: Pycnogonida) collected during the Madibenthos Expedition from Martinique shallow waters

“…The use of molecular data to perform integrative taxonomy is now routinely employed in the literature (e.g., Kantor & Puillandre 2021;Šobáňová & Ďuriš 2021;Vaga et al 2021), but surprisingly rarely for sea spiders, except for the Southern Ocean and Australia (Arango et al 2011;Dietz et al 2015aDietz et al , 2015bDömel et al 2015Dömel et al , 2017Dömel et al , 2019Dömel et al , 2020Soler-Membrives et al 2017;Brenneis et al 2020). However, this is a paramount tool to overcome the complexity of sea spider taxonomy, which enabled us to delimit additional species compared to our preparative paper (Sabroux et al 2019b) bahamensis.…”

Pycnogonida (Arthropoda) from Museu de Ciências Naturais, Rio Grande do Sul, Brazil

“…Molecular studies confirm that a complex of species exists under the name C. megalonyx. Five species and another seven cryptic species were indicated (Krabbe et al 2010;Dietz et al 2015;Dömel et al 2020). These papers suggest the use of the name C. megalonyx for specimens from South America and the Subantarctic Region, the type locality (Krabbe et al 2010;Dietz et al 2015Dietz et al , 2019.…”