Nearly all marine fish came from freshwater ancestors

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):

Fig. 1 from Vega and Wiens (2012)

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):

Polypterus senegalus, in the Polypteriformes

From the subclass (I think it’s a subclass!) Chondrostei, a chinese paddlefish:

The chinese paddlefish, Psephurus gladius

And the bowfin, the sole living species in the order Amiiformes:

The bowfin, Amia calva

______________

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

39 Comments

  1. Griff
    Posted February 16, 2012 at 6:16 am | Permalink

    It seems like a no-brainer that barriers to movement are much reduced in a marine environment compared to riverine or other freshwater environments – could differences in temperature, pressure and salinity be effective barriers? Also, wouldn’t sheer distance itself be a barrier?

    Off subject, but quite interesting:

    http://www.bbc.co.uk/nature/17028940

  2. GBJames
    Posted February 16, 2012 at 6:32 am | Permalink

    Wonderful. Truly.

  3. Hempenstein
    Posted February 16, 2012 at 7:01 am | Permalink

    All fascinating. I need to read in more detail later, but for now I just want to comment that paddlefish are so cool-looking. Never knew they came in Chinese, tho, and a different genus from the kind in the Yellowstone River (Polyodon spathula), which was formerly more widespread in N America, and from which a modest amount of caviar is processed each year in N Dakota that I’d like to try sometime.

  4. Posted February 16, 2012 at 7:11 am | Permalink

    This paper is pretty exciting in its details, but the idea that crown-group osteichthyians (the clade of actinopterygians plus sarcopterygians [= tetrapods, lungfish, and coelacanths]) is hardly new. Certain aspects of osteichthyian physiology (internal bone as a mineral store/buffer; presence of lungs as an outpouching of the gut in the basal members [enhanced for breathing in some sarcopterygians; exapted into a swim bladder in many actionopts]) have previously been considered as evidence that early bony fish spent some time in the challenging environment that is freshwater.

  5. andrewD
    Posted February 16, 2012 at 7:16 am | Permalink

    <blockquote We know from the fossil record the ancestor of all fish was marine,Do we know what the marine salinity was at this point? I presume that the salinity of the oceans has risen over time, if it was originally similar to fresh water habitats can we consider them as different. If they were similar does the marine origin of fish stand up?

    • andrewD
      Posted February 16, 2012 at 7:17 am | Permalink

      Why do I always screw up HTML?

      • GBJames
        Posted February 16, 2012 at 7:20 am | Permalink

        Because you are trying to be me?

      • Occam
        Posted February 16, 2012 at 8:08 am | Permalink

        Blame it on the white mice. It’s part of a long-term experiment they’ve been conducting on us. First, adapting to unwieldy QWERTY keyboards. Then, adapting to unwieldy HTML tags. Finally, using simulated QWERTY keyboards on WISIWYG bitmapped touchscreens to type HTML code. They’ll probably conclude that our species has no clue, besides lacking ‘free will’.

    • Diane G.
      Posted February 17, 2012 at 1:32 am | Permalink

      I hope someone who knows answers your salinity question. 🙂

  6. Ray Moscow
    Posted February 16, 2012 at 7:19 am | Permalink

    Countdown to Creationists claiming “This proves the Flood!” in 3, 2, 1 …

    (Something about all that fresh water)

    • Kevin
      Posted February 16, 2012 at 7:39 am | Permalink

      Beat me to it. You get up way earlier than I do.

      • Ray Moscow
        Posted February 16, 2012 at 7:54 am | Permalink

        Not necessarily, but I do live in England.

        • Posted February 16, 2012 at 6:42 pm | Permalink

          actually, as an ignorant question, what other than contemporary human fishing practices would be an oceanic extinction event ?

  7. J
    Posted February 16, 2012 at 7:30 am | Permalink

    Thanks for posting this, it’s fascinating stuff!

    • Diane G.
      Posted February 17, 2012 at 1:34 am | Permalink

      + 1 !

  8. Posted February 16, 2012 at 7:39 am | Permalink

    Because the basal divergences of the ray-fin phylogeny are all species-poor long branches (bichirs, paddlefish, etc.), they may reflect where ancient lineages have survived, rather than where they lived hundreds of millions of years ago. This is a general problem with inferring ancestral states of a labile character in a tree with few, deep branches. This problem does not vitiate Vega and Wiens’ conclusion, and there are ways to address the difficulty, but it is a caveat. (NB this comment is based on Jerry’s post: I’ve not gotten the paper yet.)

    • Posted February 16, 2012 at 12:32 pm | Permalink

      Indeed. In fact, their supplementary figure 2 shows pretty good evidence the most recent common ancestor of bowfins, sturgeons and other living bony fish (besides bichirs) lived in saltwater. Sure the most basal divergence is freshwater, but that’s only because both bichirs and the outgroup Cheirolepis are. I’m no paleoichthyologist, but I’m betting there are plenty of known taxa that are located by Cheirolepis but not included in their analysis which could affect the result.

  9. Achrachno
    Posted February 16, 2012 at 7:49 am | Permalink

    “marine habitat covers 70% of the Earth’s surface but contains only 15-25% of Earth’s species”

    I wonder if we’ve inventoried marine creatures well enough to know what percentage of living things they are. Samples from the sea floor are few relative to those from land or freshwater. And new things are still being found on land at a steady clip.

  10. TJR
    Posted February 16, 2012 at 8:09 am | Permalink

    Hmm, couldn’t access the paper although it seems I should have been able to.

    Is there anything on the date of this maritime extinction? Could it be the end-Permian extinction, which IIRC was particularly devastating on life in the seas?

    • Gregory Kusnick
      Posted February 16, 2012 at 10:52 am | Permalink

      That was my thought too, and the shape of the tree does seem consistent with an extinction event at around 250 Ma.

      • TJR
        Posted February 16, 2012 at 11:55 am | Permalink

        Ah yes, there is indeed a scale on the graph!

  11. Posted February 16, 2012 at 8:48 am | Permalink

    As Gregory (#8) says, these kinds of inferences are not very solid, though they are tempting to make. It could well be that the early polypteriformes lived in both saltwater and freshwater, and were simply poor competitors with later saltwater lineages, which eliminated them in saltwater. The geographic semi-isolation provided by river systems could have protected ancient, poorly-competing lineages that once occupied both salt and fresh water.

    I have not read the paper, but the tree presented here gives no information to support the author’s hypothesis. They could support it by examining fossil records (I think it might be easy to tell freshwater fossils from saltwater ones). Maybe the authors did do that–I haven’t read the actual paper.

  12. Nick Block
    Posted February 16, 2012 at 9:16 am | Permalink

    A minor quibble: the nodes are basal; taxa are not basal. There really needs to be a good term for these types of taxa, though. “Species at the tips of long branches that lead to more basal nodes” is a tad unwieldy. 🙂

    • whyevolutionistrue
      Posted February 16, 2012 at 9:33 am | Permalink

      Criticism accepted, thanks.

      • Joe Dickinson
        Posted February 16, 2012 at 3:26 pm | Permalink

        I’ve always had a problem with this basal/crown group distinction. If you were an intelligent Polypteriformian, wouldn’t you think of everything below the top branch as basal (to you). In other words, “basal” seems to be a matter of perspective rather than objective reality.

  13. Tyro
    Posted February 16, 2012 at 9:27 am | Permalink

    Wow, wonderful. Makes me want to read more! I’ve read a little bit about some of the adaptations of species like salmon who have a mixed freshwater/saltwater life and it always fascinated me.

    Now if only someone could write a book about it.

  14. Charles Jones
    Posted February 16, 2012 at 10:34 am | Permalink

    Like many now-dominant animal clades, the ray-finned fishes radiated following a major mass extinction event.

    In this case, the extinction event took place at the end of the Devonian, about 375 Myr ago. Like other mass extinction events, it took out the dominant groups, which at the time were fishes with bony plates in their heads. There is no evidence that I’m aware of that early sharks or ray-finned fishes were increasing their diversity approaching the extinction event, and thus no evidence that they were out-competing the old fish lineages. Instead, some external set of circumstances caused the mass extinction.

    What I find interesting is that perhaps the ancestors of modern ray-finned fishes escaped extinction because they were not living in the oceans. Instead they happened to be living in fresh-water refuges and thus survived to seed a new branch of the tree of life.

    The fossil record of these fishes in Jerry’s post does not extend back to the Late Devonian, but Michael Benton’s phylogenic trees infer ancestors originating back at this time (Vertebrate Paleontology, 3rd edition).

    • Gregory Kusnick
      Posted February 16, 2012 at 11:00 am | Permalink

      Actinopterygians may have originated post-Devonian, but in the tree diagram shown here, essentially all of the radiation and re-invasion of saltwater takes place post-Permian.

  15. Posted February 16, 2012 at 11:41 am | Permalink

    Isn’t low number of species in the oceans possibly linked to the low number of taxonomists in the ocean?

    • Achrachno
      Posted February 16, 2012 at 9:48 pm | Permalink

      That’s another way of asking the question I asked above. It’s difficult to survey marine organisms compared to terrestrial ones, and we still have lots to do with the terrestrial stuff. I imagine we’re near ignoramuses under the sea.

  16. Posted February 16, 2012 at 1:11 pm | Permalink

    In Ordovician times when these pre-fish were evolving, the Oceans covered the whole surface of the Earth – Pannotia – and sedimentary sheets which were deposited were continuous and also covered the whole Earth. When these sheets broke up into slabs by movement of the underlaying basement rock, the water drained down into the gaps between them to form the first separate seas, and dry land areas. It is likely that water gradually became saline over more recent times, geologically speaking. The fish will have had to gradually adapt to this increasing brininess of the oceans. Have a look at my Planmet Channel on Youtube where I have videos which describe this.

    • Griff
      Posted February 17, 2012 at 1:25 am | Permalink

      Uh huh. I see. So Gondwana never existed?

      Methinks “a little too much LDS”

  17. ChasCPeterson
    Posted February 16, 2012 at 1:20 pm | Permalink

    marine ray-finned fish, which to an approximation means all marine fish, derive from ancestors that were freshwater. And that’s surprising.

    Not to a physiologist. Marine actinopts regulate their body fluids at a solute concentration (300-400 mOsm) that is very similar to that of freshwater fishes (250-300; same as tetrapods) and closer to freshwater (<2 mOsm) than seawater (1000 mOsm), and they have to spend a lot of energy to do it. No marine invertebrate does that, and neither do hagfish.

    • Filipe
      Posted February 16, 2012 at 3:27 pm | Permalink

      Yes, that is the argument I’ve always seen advanced as evidence of fresh water origin (that and the swimming bladder). Similar thing for sharks and rays (the use urea to maintain osmotic equilibrium was opted when their ancestors went back to the sea).

    • Loren Petrich
      Posted February 17, 2012 at 9:50 pm | Permalink

      I remember seeing the solute-concentration argument long ago, and I find it rather satisfying to see an independent line of work converge on it.

      There is a problem: the divergence of ray-finned fish from other jawed vertebrates is some 200 million years before. What’s in that gap?

  18. Jim Thomerson
    Posted February 16, 2012 at 3:28 pm | Permalink

    There are various estimates that about 40% of fish species are freshwater. Freshwater is what, about 1% maybe, of total liquid water? Shore fishes, coral reef, mangrove, etc. make up a bit larger percentage, and open water oceanic fishes maybe less than 5%. It looks like it is a matter of geographical isolation, and allopatric speciation. Whether these figures will hold up into the future is conjectural. As a mostly fresh water ichthyologist, I am biased to think that the number of undescribed freshwater species is larger than, or at least compares with, the number of undescribed marine species.

    The use of DNA methodology is going to help out in groups where there are a number of morphologically similar species. When we revised Austrofundulus in 1978, we took four species, including two subspecies down to two species, based on morphology. Recently we revised Austrofundulus again, with the aid of DNA data, and now recognize seven species.

  19. Posted February 16, 2012 at 3:32 pm | Permalink

    Cognitive. Dissonance.

    I just started reading John Long’s The Rise of the Fishes (http://www.amazon.com/Rise-Fishes-Million-Years-Evolution/dp/0801854385). I guess I should read the new paper first…

  20. W.Benson
    Posted February 16, 2012 at 5:40 pm | Permalink

    “Don´t know much about algebra,
    Don’t know what a slide rule is for,
    But I do know that one and one is two,”
    except with logarithms.
    (“Wonderful World”, Sam Cooke)

    Fig. 1b is tragic. The abundance scale for total species in each lineage is logarithmic, whereas the relative proportions of salt vs fresh-water are arithmetic. If you did not read the legend, you might wrongly conclude that salt water Polymixiiformes are vastly more speciose that salt water Astaniophysii. The absolute number of salt water species in these is about 10 and 100, respectively.

    With regard to Indo-Pacific marine diversity, seas in the region are often shallow and parts (enclosed seas) may be subject to isolation by sea-level changes and tectonics.

    Interesting stuff.

    • TJR
      Posted February 17, 2012 at 3:33 am | Permalink

      Well spotted, I missed that (as indeed I missed the scale entirely on Fig 1a).

      A log scale isn’t so bad if you’ve got two adjacent bars for freshwater and marine, but to do it as stacked bars is wildly misleading.


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