Phylogeny and evolution of corambid nudibranchs (Mollusca: Gastropoda)

Abstract

Organismic diversity, as well as distributional and ecological patterns, can be fully understood in an evolutionary framework only. Reliable phylogenetic trees are required to 'read history', but are not yet available for most marine invertebrate groups. Molecular systematics offers an enormous potential, but still fails for 'all-species approaches' on groups with species that are rare or occur in remote areas only, simply because there is no easily collectable material available for sequence analyses. Exploring morphologically aberrant corambid nudibranch gastropods as a case study, we assess whether or not morphology-based phylogenetic analyses can fill this gap and produce a tree that allows a detailed view on evolutionary history. Morphology-based parsimony analysis of corambids and potential relatives resulted in a well-resolved and remarkably robust topology. As an offshoot of kelp-associated onchidoridid ancestors, and obviously driven by the heterochronic shortening of life cycles and morphological juvenilization in an ephemeral habitat, the ancestor of corambids originated in cool northern Pacific coastal waters. A basal clade (the genus Loy) diverged there, adapting to live on soft bottoms under successive reversals of paedomorphic traits. The more speciose Corambe lineage radiated preying upon short-lived encrusting bryozoa in a high-energy kelp environment. Selection favoured transformation of the mantle into a cuticle-covered shield, and successive paedomorphic translocations of dorid anal gills to the protected ventral side of the body, where compensatory, multiple gills evolved. Corambe species probably first colonized tropical American seas, and then radiated in worldwide temperate waters: this is explained by the excellent long-distance dispersal abilities afforded by rafting on kelp, with the subsequent divergence of colonizers in allopatry. The competitive coexistence of Corambe pacifica MacFarland &O'Donoghue, 1929 and Corambe steinbergae (Lance, 1962) off California is the result of independent colonization events. The closing of the Isthmus of Panama separated the latter species from a flock that have radiated within warm Atlantic waters since then. Our case study shows that morphological structures, if investigated in depth, bear the potential for an efficient phylogenetic analysis of groups that are still elusive to molecular analyses. Tracing character evolution and integrating a wide range of geographic, biological, and ecological background information allowed us to reconstruct an evolutionary scenario for corambids that is detailed and plausible, and can be tested by future molecular approaches.

Family matters: The first molecular phylogeny of the Onchidorididae Gray, 1827 (Mollusca, Gastropoda, Nudibranchia)

“…Even though previous morphological investigations have been conducted (Fahey and Valdés, 2005;Martynov and Schrödl, 2011;Millen and Martynov, 2005), no additional members of the Phanerobranchia were represented, and relationships regarding the Onchidorididae have resulted in weak support between genera, as well as the family's placement in the Suctoria. A molecular phylogeny focused on a diverse sampling of genes and taxon could aid greatly in the understanding of family relationships, clarify homoplasies within the family, and potentially gain insight into the complexity of dorid gill evolution and the diversification of reproductive morphology.…”

“…(Fahey and Valdés, 2005;Martynov and Schrödl, 2011;Martynov, 2011;Millen and Nybakken, 1991;Millen and Martynov, 2005). Representatives of some genera display gill morphology similar to the Cryptobranchia, referred here as the ''cryptobranch condition'', but this arrangement is not considered to be homologous (Millen, 1985).…”

“…1) (Fahey and Valdés, 2005;Martynov and Schrödl, 2011;Millen and Martynov, 2005). Molecular studies that have involved the Onchidorididae have been inadequate in estimating a definitive placement of family in the Nudibranchia and relationships between the genera (Wollscheid-Lengeling et al, 2001;Hallas and Gosliner, unpublished).…”

“…In addition, they constructed the Akiodorididae, consisting of five genera previously thought to be members of the Onchidorididae, which, at times, have also been placed into the Goniodorididae (Bergh, 1883;Høisaeter, 1986;Odhner in Franc, 1968;Thiele, 1931). Moreover, the Goniodorididae have also been consistently recovered nested in the Onchidorididae, but no taxonomic revision has been proposed due to the low support and sparse taxon sampling (Fahey and Valdés, 2005;Martynov and Schrödl, 2011;Millen and Martynov, 2005).…”

“…Members of the Suctoria (=Onchidoridoidea) have been traditionally allied, and morphological studies have shown that they are closely related, however weakly supported (Fahey and Valdés, 2005;Martynov and Schrödl, 2011;Millen and Martynov, 2005). Millen and Martynov (2005) recovered Corambidae nested in Onchidorididae sister to Adalaria and combined the two families under the latter.…”