Subterranean beetle speciation down under
Hello there dear friends of the cave beetle, I hope this is reaching all of you well as this challenging year draws to an end, leaving many challenges to leap over into the next one. Besides the major ones concerning all of us, it seems like I succeeded in deferring the write up of the cave beetle temperature tolerance data into 2021. Not proud of it. But it is what it is. And glad to defer the blame partly on being distracted by yet again another fantastic cave beetle study that deserves to be shared here. This note needs to rave about new work from Steven Cooper's lab that just came out: "Evidence for speciation underground in diving beetles (Dytiscidae) from a subterranean archipelago" (Langille et al. 2020). You may remember Steve's work on oxygen uptake from water in the amazing subterranean diving beetles of the Yilgarn region in Western Australia we covered in August: https://experiment.com/u/kfY4pA.
In the new study, Steve's group addressed a classic question in cave biology: How did the diversity of species that inhabit subterranean habitats nowadays come about? More precisely, in many cases not only a single species populates a specific subterranean environment. Instead, we find different yet closely related species inhabiting adjacent subterranean habitats. Best known to us, of course, is the hirtus-species clade with its 18 relatives of P. hirtus in different caves of Alabama, Georgia, Kentucky, and Tennessee (Leray et al. 2019). In the case of the subterranean diving beetles of the Yilgarn region, we are looking at more than 100 closely related species (Balke et al., 2004; Watts and Humphreys, 2006; Watts and Humphreys, 2009). Moreover, in some of their aquatic subterranean habits, i.e. aquifers, not only one but up to 3 species are present.
There are two basic scenarios how this distribution of subterranean diving beetle diversity may have come about. One is that the species had already split as regular surface species before being forced into the subterranean realm by events such as climate change. Alternatively, the latter transition occurred only once in a last common ancestor which then gave rise to new species in the subterranean environment. Past work suggests that the above-ground speciation scenario is likely the most common process. This, for instance, is the best explanation for the distribution of hirtus-cluster species (Leray et al. 2019), all of which inhabit separate caves and which, as we just learned from Kirk Zigler's work, migrate between caves just very rarely (Balogh et al., 2020). On the other hand, there are these cases of multiple diving beetle species in some of the Australian aquifers, which can be imagined to have diversified within the shared subterranean environment. Indeed, this possibility was further supported by phylogenetic analyses which revealed that aquifer-sharing diving beetle species are most closely related to each other in the overall diversity of Yilgarn diving beetle species (Leijs et al., 2012).
However, while intriguing, it has been challenging to think about how speciation would occur in such a relatively small amount of space where individuals are bound to mingle more than being persistently separated from each other which could culminate into speciation. Secondly, the three species may still have split up before aridification, i.e. climate change, in the Yilgarn region and then become trapped in the same aquifer because of their initial close association above ground.
To test between these scenarios, Steve's group had the fantastic idea to look at genetic changes that are predicted to have occurred in different patterns pending the surface vs subterranean speciation scenarios. Like many subterranean species, the subterranean diving beetles lost their compound eyes suggesting the correlated degeneration of vision-specific genes. The precise nature of these genetic changes in turn could shed new light as diagnostic tools on the speciation histories of the aquifer-sharing species. If the species separated from each other above ground before individually adapting to the lack of light underground, they are expected to have accumulated different degenerative mutations in their vision genes during the subsequent persistence in darkness. If, by contrast, speciation happened underground following aquifer colonization by their last common ancestor and if subsequently also eye loss preceded their speciation underground, then all three species would be characterized by shared deleterious mutations in their vision genes, inherited from their last common ancestor underground.
As you can see, that is a lot of "ifs" but Steve's group just couldn't resist and took the chance. In total, they investigated the sequences of three vision genes: long wavelength opsin, arrestin 1, and arrestin 2. Most gratifying is what they found in the case of the three species with the handy names Paroster macrosturtensis, Paroster mesosturtensis, and Paroster microsturtensis that co-reside in the aquifer by the name of Sturt Meadows:
The three aquifer colocals share identical, fairly massive sequence deletions in their opsin and arrestin 2 genes. The one in the opsin gene looks like this in comparison to the opsin sequences of species in other aquifers:
Moreover, the three species also share a single nucleotide mutation in the arrestin 1 gene that results in the truncation of the resulting protein. Combined, these shared deleterious mutations leave no doubt that P. macrosturtensis, P. mesosturtensis, and P. microsturtensis inherited these gene function compromising mutations from a last common ancestor that had adapted to the darkness of aquifer life. And that means their speciation occurred underground.
While there are interesting questions arising exactly how speciation occurred underground, the data produced in this work are the most direct evidence today that speciation can occur in subterranean habitats in addition to the more conventional above-ground scenarios.
Great way to close out 2020 subterranean diving beetle pioneers down under!
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