Speciation with gene flow in marine systems

Abstract

Over the last century, a large body of literature emerged on mechanisms driving speciation. Most of the research into these questions focussed on terrestrial systems, while research in marine systems lagged behind. Here, we review the population genetic mechanisms and geographic context of 33 potential cases of speciation with gene flow in the marine realm, using six criteria inferred from theoretical models of speciation. Speciation with gene flow occurs in a wide range of marine taxa. Single traits, which induce assortative mating and are subjected to disruptive selection, such as differences in host-associations in invertebrates or colour pattern in tropical fish, are potentially responsible for a decrease in gene flow and may be driving divergence in the majority of cases. However, much remains unknown, and with the current knowledge, the frequency of ecological speciation with gene flow in marine systems remains difficult to estimate. Standardized, generally applicable statistical methods, explicitly testing different hypotheses of speciation, are, going forward, required to confidently infer speciation with gene flow.

Genomic signatures of host‐associated divergence and adaptation in a coral‐eating snail, Coralliophila violacea (Kiener, 1836)

“…Genome‐wide SNP data from six sympatric populations of C. violacea revealed two clearly differentiated clusters that were largely concordant with coral host, consistent with results from mitochondrial DNA (Simmonds et al, ). As with insects (Jean & Jean‐Christophe, ; Simon et al, ), this genome‐wide differentiation supports the conclusion of ecological divergence based on host association and adds to a small but growing literature on ecological divergence in marine environments (Fritts‐Penniman et al, ; Potkamp & Fransen, ; Titus, Blischak, & Daly, ).…”

“…Jean & Jean-Christophe, 2010;Simon et al, 2015), this genome-wide differentiation supports the conclusion of ecological divergence based on host association and adds to a small but growing literature on ecological divergence in marine environmentsPotkamp & Fransen, 2019;Titus, Blischak, & Daly, 2019).While SNP data reveal significant divergence between host-specific lineages of C. violacea, divergence was substantially lower in genome-wide SNPs compared to mtDNA (F ST = 0.047 vs. Φ CT = 0.561).This result may partially be a function of the smaller effective population size of the mitochondrial genome(Palumbi, Cipriano, & Hare, 2001). However, lower divergence values also suggest intermediate levels of gene flow between distinct host-associated lineages (Nm>10), values that are similar to other cases of sympatric host-associated divergence (e.g.,Gouin et al, 2017;Peccoud, Ollivier, Plantegenest, & Simon, 2009;Smadja et al, 2012).…”

“…Evidence from traditional genetic markers (i.e., microsatellites, RFLPs, allozymes, nuclear, mitochondrial, and ribosomal genes) demonstrates the potential for ecological speciation in marine taxa exhibiting symbiotic relationships (Bowen et al, ; Miglietta, Faucci, & Santini, ; Peijnenburg & Goetze, ; Potkamp & Fransen, ), including amphipods on macroalgae (Sotka, ), coral‐dwelling barnacles (Tsang, Chan, Shih, Chu, & Allen Chen, ), coral‐eating nudibranchs (Faucci, Toonen, & Hadfield, ; Fritts‐Penniman, Gosliner, Mahardika, & Barber, ), parasitic snails (Gittenberger & Gittenberger, ; Reijnen, Hoeksema, & Gittenberger, ), anemone‐associated shrimp (Hurt et al, ), anemone fish (Litsios et al, ), and coral‐dwelling gobies (Duchene, Klanten, Munday, Herler, & van Herwerden, ; Munday, van Herwerden, & Dudgeon, ). While encouraging, there are gaps in our knowledge that with the expansion of genomic technologies, we are now in a position to begin to fill.…”

Evolution and biogeography of the Zanclea-Scleractinia symbiosis

“…This could be due to the very likely fact that the diversification of extant coral genera occurred much earlier than the radiation of extant coral-associated Zanclea. One of the main mechanisms underlying Zanclea radiation, acting both alone and in conjunction with geography-related processes, may be host-switching to exploit new resources and subsequent specialisation of the association and reproductive isolation, as shown in other coral-associated taxa (see review by Potkamp and Fransen 2018). This scenario may apply especially for specialist Zanclea clades.…”

A synoptic review of the family Dendronotidae (Mollusca: Nudibranchia): a multilevel organismal diversity approach

“…Until now there are no unequivocal and universal criteria for species delimitations when the underlying evolutionary processes and phylogenies are taken into consideration (e.g., Zachos et al, 2013;González et al, 2018;Stanton et al, 2019;Platania et al, 2020), and even for the existence of species at all (Ereshefsky, 1998;Willis, 2017;Reydon & Kunz, 2019). At the conceptual level, more than 26 different species concepts have been suggested (Zachos, 2016) but at a practical level even the most widely acclaimed criterion of reproductive isolation (Mayr, 1969(Mayr, , 1982 is not robust as has been shown on numerous occasions (e.g., McDonald and Koehn, 1988;Mallet, 2005;Kijewski et al, 2006;Harrison & Larson, 2014;Jančúchová-Lásková et al, 2015;Crossman et al, 2016;Fraïsse et al, 2016;Potkamp & Fransen, 2019).…”