I’m sure that most of us think that marine fish evolved in the sea, but a new paper by Greta Vega and John Wiens in the Proceedings of the Royal Society (B) says that that just ain’t so. The vast majority of them evolved from ancestors who lived in fresh water (themselves derived from marine ancestors) and then re-invaded the sea—just as marine mammals evolved from terrestrial mammals whose distant ancestors were aquatic.
As Vega and Wiens point out, compared to the land, the sea is biologically depauperate: marine habitat covers 70% of the Earth’s surface but contains only 15-25% of Earth’s species. It gets worse if you count “habitable space”: since the ocean is three-dimensional, Vega and Wiens claim that it contains “90-99% of the volume of the habitable biosphere.”
Why this relative lack of marine species compared to those on land (or freshwater)? A number of hypotheses have been proposed, including the water habitat itself (this doesn’t stand up because freshwater fish are far more diverse per unit area than marine fish), and a greater net primary productivity (NPP: the amount of atmospheric carbon that finds its way into plants) in terrestrial than marine habitats. (NPP is the base of the biological food pyramid.) But the difference in NPP between terrestrial and marine habitats is not very large, and freshwater NPP is by far the lowest despite having more fish diversity than marine habitats.
My own guess, which is also that of Vega and Wiens, is that geographic barriers, which are the first step in most speciation events, are simply less common, or arise less frequently, in open water than in terrestrial habitats (riverine fish, of course, are geographically isolated in river systems). It’s telling that the greatest diversity in the ocean is found in the Indo-Pacific, which Vega and Wiens describe as “geographically complex,” limiting dispersal and facilitating the formation of new species.
Vega and Wiens try to resolve this issue by doing a DNA-based phylogeny of the actinopterygians (the ray-finned fish, so called because of the bony struts in their fins). Ray-finned fish are by far the most numerous of all “fish”—about 96% of them. What they found was surprising: here’s the phylogeny of different actinopterygian groups and the number of species in each group , with the colors indicating where they live (red is freshwater, blue marine, and mixed colors indicating that members of the group occupy both habitats. Notice that the three “basal groups”, Polypteriformes, Chondrostei, and Amiiformes, are all exclusively freshwater (click to enlarge):
The completely freshwater nature of the basal (and hence oldest) actinopterygians indicates that all the others came from freshwater ancestors. And that means that every ray-finned fish in the sea derived from freshwater species.
We know from the fossil record the ancestor of all fish was marine, so what has happened here is that the sea is populated with things that came from freshwater, but whose ancestors themselves originally came from the sea. I’m not sure whether actinopyterygians themselves evolved in the sea (Vega and Wiens suggest no, but one expert I consulted said they probably did), but if the answer is “no” it probably means that there was an extinction event that wiped out marine actinopterygians and perhaps other groups as well. Then freshwater actinopterygians re-invaded the empty sea and repopulated it.
Vega and Wiens speculate that such an extinction event, whatever groups it decimated, helps account for the lack of marine biodiversity, though they don’t present independent evidence for such an event. It may just be that the equilibrium number of all species in the ocean is lower because they are formed less frequently due to the lack of geographic barriers. If extinction rates are comparable in terrestrial and marine environments, but speciation rates are lower in marine habitats, then the equilibrium number of species will also be lower in the sea.
This is all speculation, but what does seem solid from the Vega and Wiens paper is that marine ray-finned fish, which to an approximation means all marine fish, derive from ancestors that were freshwater. And that’s surprising.
You may wonder what fish are in those three freshwater “basal” groups. Here’s an example of each.
From the order Polypteriformes, or bichirs, a group of bizarre fish with primitive traits (note the subdivided dorsal fin, unique in this group):
From the subclass (I think it’s a subclass!) Chondrostei, a chinese paddlefish:
And the bowfin, the sole living species in the order Amiiformes:
Vega, G. C. and J. J. Wiens. 2012. Why are there so few fish in the sea? Proc Roy. Soc. Lond. B: online, doi:10.1098/rspb.2012.0075