Sculpins Go Wild

Yokoyama, A., & A. Goto. 2005. Evolutionary history of freshwater sculpins, genus Cottus (Teleostei; Cottidae) and related taxa, as inferred from mitochondrial DNA phylogeny. Molecular Phylogenetics and Evolution 36 (3): 654-668.

Freshwater sculpins of the genus Cottus are a widespread Holarctic group of smallish fishes, belonging to the suborder Cottoidei (the image at top, from Wikimedia, shows Cottus gobio). While most members of the Cottoidei are marine, there are a number of freshwater taxa - about 40 species in Cottus, three in Myoxocephalus (a genus also including marine species), the monotypic genera Mesocottus and Trachidermus, and 33 species divided between three families and 12 genera found in Lake Baikal in central Siberia. Species of Cottus show a wide diversity of life histories, from catadromous (species that live in fresh water before travelling to the sea to spawn) to amphidromous (species that can move between fresh and salt water, but don't do so specifically to spawn - the amphidromous Cottus species are freshwater spawners) to species that are permanently freshwater. As such, Yokoyama and Goto (2005) investigated the phylogeny of this genus using the mitochondrial 12S rRNA and CR (control region) genes to discover its biogeographical history and how the different life histories have evolved.

Previously, the catadromous life cycle has been thought to be ancestral for Cottus, both because freshwater cottoids as a whole are certainly derived from marine ancestors, and because the catadromous Trachidermus fasciatus was identified on morphological groups as the sister group to Cottus. The amphidromous lifestyle was thought to have arisen next, from which increasing specialisation for freshwater habitats had given rise to the purely fluvial (river) or lacustrine (lake) species. The results of Yokoyama and Goto did not contradict the basal position of catadromy, but added a twist - the single catadromous species, Cottus kazika, did not group with the remaining Cottus species, but instead was sister (with high support) to Trachidermus fasciatus, making Cottus polyphyletic (Shedko & Miroshnichenko (2007) have since moved C. kazika out of Cottus as a result, resurrecting an old genus name to label it Rheopresbe kazika). The role of catadromy in the evolution of Cottus therefore becomes a bit more uncertain.

The remaining, freshwater-spawning species of Cottus were supported as a clade, admittedly with low support though the shared life history makes the clade credible. As for whether the amphidromous life style was indeed ancestral to the purely freshwater, Yokoyama and Goto's results seemed to suggest the exact opposite, with the amphidromous species scattered through the various clades of purely freshwater species, and not particular basal within those clades. However, the authors themselves were a little more agnostic about their results - they point out that repeated parallel loss of amphidromy could give a falsely parsimonious appearance of derived amphidromy. Biogeography-wise, their results supported the traditional view of an origin of Cottus somewhere in eastern Eurasia, where the greatest diversity of species is found. Four reasonably well-supported clades of freshwater-spawning species were identified - two restricted to eastern Eurasia and Japan, one found across Eurasia, and one (their clade E) including both Eurasian and North American species.



The non-monophyly of Cottus goes further than just one wayward species, though. You recall that I mentioned the diverse fauna of freshwater cottoids endemic to Lake Baikal? In the past, species of this fauna were divided between three families - some in Cottidae with the other freshwater sculpins, some in an endemic family Abyssocottidae, and a separate family for the unique genus Comephorus. However, molecular analysis (Kontula et al., 2003) had discovered that the Baikal cottoids formed a single clade, and had probably originated from a single colonisation of the lake by an ancestral species. Once in the lake, the cottoids had diversified rapidly (molecular clock calculations, for what they're worth*, estimate an age of 1.2 to 6.2 million years for the Baikal radiation) to occupy a number of niches, including some not occupied by sculpins anywhere else in the world. The pictures above give some indication of the diversity of Baikalian cottoids - the pelagic Cottocomephorus inermis (from here) on the right, an unidentified benthic species reasonably similar to a typical cottid (from here) in the centre, and the highly derived pelagic Comephorus on the left (image from here).

*Okay, so I don't trust molecular clocks as far as I can throw them or the researchers who calculate them. In this case, unfortunately, they're all the evidence we have.

The point where it all becomes really interesting, though, is that not only does this diversity derive from a single point, but it is actually nested within the genus Cottus! This had previously been suggested by Kontula et al. (2003), and so Yokoyama & Goto (2005) took the opportunity to test Kontula et al.'s results against their more extensive dataset by including the data from the earlier study. While support was not impressive, the Baikalian radiation seems to be nested within Yokoyama & Goto's clade E.

As usual, though, I did come away from this paper with a few questions. Yokoyama and Goto used only one marine species and a member of Myoxocephalus as outgroups, and while they did find the Trachidermus + Rheopresbe clade as sister to the freshwater-spawning clade, support was very low and the position was not statistically supported. Is there actually a direct connection between these two clades, or did the catadromous species gain their freshwater lifestyle independently from the freshwater species? Answering this question will be vital to understanding what (if any) role catadromy may have played in the transition of the ancestors of Cottus from marine to freshwater habitats. And what of the untested freshwater Mesocottus haitej? Does this Siberian species represent another independent movement into freshwater, or does the paraphyly of Cottus extend even further?

REFERENCES

Kontula, T., S. V. Kirilchik & R. Väinölä. 2003. Endemic diversification of the monophyletic cottoid fish species flock in Lake Baikal explored with mtDNA sequencing. Molecular Phylogenetics and Evolution 27 (1): 143-155.

Shedko, S. V., & I. L. Miroshnichenko. 2007. Phylogenetic relationships of sculpin Cottus volki Taranetz, 1933 (Scorpaeniformes, Cottidae) according to the results of analysis of control region in mitochondrial DNA. Voprosy Ikhtiologii 47 (1): 27-30 (transl. Journal of Ichthyology 47 (1): 21-25).