Hybrid speciation in Galápagos finches

I’ll take “speciation” in this post, as do all the authors involved, to mean “the origin of reproductive barriers between populations that live in the same area, preventing them from either cross-mating or producing fertile hybrids if they do.” Most biologists think that speciation—the acquisition of these barriers—requires a prolonged period of geographical isolation between populations, allowing them to diverge through natural selection or genetic drift without contamination of genes between the groups. When that differentiation has proceeded to a certain point, reproductive barriers can arise as a byproduct of evolutionary divergence, and thus we have new species. (If we’re to be sure they are genuine “biological species”, they should be able to coexist after coming back together in the same area, or, in a one-way test, produce sterile or inviable hybrids when forcibly mated in zoos. If they’re cross-fertile in zoos, we can’t tell, for lots of animals that coexist in the wild without hybridizing can do so under the artificial conditions of confinement.)

This process, which Allen Orr and I described at length (and adduced evidence for) in our book Speciation, takes time—often lots of it. We estimated that producing a new species in this way in sexually-reproducing organisms takes on the order of a million years.

Yet there are ways that speciation can go faster—much faster. One way is “hybrid speciation”, in which two species have a rare bit of gene exchange, and that leads to the formation of a hybrid population that’s genetically heterogeneous. That population, faced with an odd genetic admixture and perhaps strong selection on a novel genome, might itself evolve to become reproductively isolated from both parental species, thus forming a third hybrid species.

This happens a lot in plants through the process of allopolyploidy (see here), which has accounted for a few percent of speciation events in some plant groups (and more in ferns). This form of speciation stands out for two reasons: it’s quick, often taking just a handful of generations, and it occurs without the need for geographical isolation of populations, since it’s begun by a rare hybridization event between coexisting species.  No evolutionists doubt the importance of allopolyploidy as a way of forming plant species.

Another and similar method, but not involving doubling of chromosome complements, is “homoploid hybrid speciation”, in which two normal diploid species, like the case described below, hybridize and, because some of the hybrids may be fertile or semifertile, those diploid hybrids can evolve quickly into a new species that is reproductively isolated from both parent species. (Note that in these cases the parental species can’t be absolutely reproductively isolated, as they have to mate and some of the hybrids have to be fertile. But, as Allen and I noted, the definition of “species” can allow for some trivial gene flow.)

In recent years homoploid hybrid speciation has been highly touted by some biologists, but, as I noted about a year ago, hard evidence for the process is rare. A 2014 paper in Evolution, using stringent criteria to examine possible cases, found only four reasonably convincing instances of this kind of speciation: three in a single genus of sunflowers, and one in butterflies. So the process, while interesting, has yet to be shown sufficiently common to constitute an important new take on how species arise.

But a new paper in Science by Sangeet Lamichhaney et al. describes what seems to be another case, this time occuring in the Galápagos finch genus Geospiza. The paper, which is a good one, has received a lot of press, some of it misleading, implying that this process could be common or that the concept of “biological species” is worthless. But the Science paper itself doesn’t say that.  The reference to the paper is at the bottom, but it’s behind a paywall. Judicious inquiry might get you a copy, though.

What it shows is that a new and very small species of finches arose on the Galápagos island of Daphne Major after a stray finch from another island made it to Daphne and mated with a local, resident species. This mating gave rise to a population that appears to be reproductively isolated from at least one parental species, and perhaps from the other. This isolation evolved in three generations or so, and thus the speciation event was very quick.

The story. A juvenile male of the large cactus finch G. conirostris, resident on the island of Española (and a small satellite island), flew more than 100 km to land on the tiny island of Daphne Major. Here’s a large cactus finch and the proposed journey that male took, bypassing at least two other islands to get to Daphne Major:

Geospiza conirostris, the large cactus finch

The hypothetical flight path, taken from the paper, which explains the route.

Once on Daphne, the male mated with a female of the local species: G. fortis, the medium ground finch. Here’s a female. Note that her bill (and also her body, which you can’t tell) is considerably smaller than that of the cactus finch, which has a massive, deep bill.

Female, G. fortis

One of the big findings of this paper, achieved through genetic analysis, was that the errant male parent was a G. conirostris rather than a G. scandens (common cactus finch), which initially seemed more likely because G. scandens lives on the much closer island of Santa Cruz. What the newspapers that described the research usually failed to add was that this hybrid population and its isolation has been known for some time and the observations have been published (there have been no observations since 2012). The real novelty of the Science paper is the fact that the identity of one founding parent was a surprise, and that it flew over 100 km to get to Daphne Major.

The G. fortis X G. conirostris mating produced one female and four male hybrids. One male mated with another local G. fortis female, while another male mated with his hybrid sister. From then on, every bird descending from that first hybrid coupling mated incestuously, within the lineage, and this has been going on for six generations. As of 2012, this inbred population has formed a closed mating group that is tiny: eight breeding pairs and 23 individuals. Here’s the lineage showing the immigrant male (right), his female mate, and the offspring and who they mated with. After the first mating between hybrid 17870 and outsider G. fortis 15170, all matings have been incestuous—within the group:

We have then, a population whose members mate only with other members. That indicates some reproductive isolation from the local species (there are three, including G. fortis), but of what kind?  The authors posit three types of isolation:

1.) Sexual isolation. The physical appearance of the hybrid finches makes them undesirable as mates for the other G. fortis individuals, for their beaks and bodies are bigger. Finches choose mates partly based on their appearance, as they learn a “proper” appearance by imprinting on their parents. Although imprinting is based on “cultural” exposure and not specific genes that code for “mate with an individual having a big body and beak”, this produces mate discrimination based on genetic differences between the species, and thus can be considered true reproductive isolation.

2.) Another form of sexual isolation: song differences. We know that in the Galápagos finches the males learn their song by imprinting on or imitating their fathers (this is known from natural cross-fostering studies), and it’s likely that females, too, learn the “appropriate” song of a mate by hearing their father, and thus mate with a male having her dad’s song. Since these males sing a song different from that of either parental species, the hybrid females would tend to mate with hybrid males, perpetuating the incestuous lineage.

3.) There is ecological isolation. The deeper, stronger beaks of the hybrid population enables them to open the tough, woody fruits of Tribulus cistoides  (the “fever plant” or “puncture vine”), especially in the dry season when food is scarce. This allows some ecological segregation due to differential resource use, but also allowed the hybrid population to at least hang on to a tenuous existence on Daphne Major.  Here are some T. cistoides plants and woody fruits:

 

 

But is this species reproductively isolated from the distant species G. conirostris on Española? If it isn’t, it’s not a true biological species. We don’t know the answer because the hybrid “species” doesn’t encounter the population on Española. This is crucial, because it’s not a new species unless the hybrid species is reproductively isolated from both parental species. The authors admit that this is “unknown” but guess that isolation from G. conirostris is “likely” because of the difference in bill size, body size, and song. But this is speculative.

There are other interesting data in the paper, too, but they need not detain us here. The important result is that we probably have a very sparse hybrid species of bird, that it formed in about three generations, and we now know exactly which species were the parents.

It’s another question whether this new species will persist. I suspect it won’t because it’s very small and may be wiped out either by demographic stochasticity (fluctuations in population size) or by another cross-breeding event with G. fortis that could cause the new species to be “mated to death”.  But species concepts aren’t prospective: we don’t say a reproductively isolated population isn’t a species because it’s liable to go extinct. For, in the end, virtually all species go extinct without leaving descendants.

As for what this paper says about the ubiquity of homoploid hybrid speciation, well, not much. We had four good cases and now we have five, though you wouldn’t know of this paucity by reading the popular press. The only statement I object to in this very nice paper is its very last sentence, “Joint occurrence of rare and extreme events such as these may be especially potent in ecology and evolution.” But if they’re rare and extreme, why are they “potent”? They’re surely interesting, but don’t suggest for a second that these speciation events somehow change our view of how new species form.

h/t: Dom, j.j.

________

Lamichhaney, S., F. Han, M. T. Webster, L. Andersson, B. R. Grant, and P. R. Grant. 2017. Rapid hybrid speciation in Darwin’s finches. Science, online  23 Nov 2017. DOI: 10.1126/science.aao4593
eaao4593. DOI: 10.1126/science.aao4593

26 Comments

  1. Posted November 26, 2017 at 10:50 am | Permalink

    Reblogged this on The Logical Place.

  2. Bruce Lyon
    Posted November 26, 2017 at 10:52 am | Permalink

    I saw Rosemary Grant give a talk a last summer that included this work, among lots of other findings from the project. She indicated that Jerry’s colleague at Chicago, Trevor Price, was the graduate student who caught the first bird of the lineage (Big Bird) and I think at the time Trevor realized that the bird was really different.

    • Posted November 26, 2017 at 11:01 am | Permalink

      Yes, I talked to Trevor before I wrote this piece, just to make sure my facts were right.

  3. Eric Schultz
    Posted November 26, 2017 at 11:00 am | Permalink

    Another possible case of hybrid speciation, on a broad spatial scale:
    Wilcox, C. L., H. Motomura, M. Matsunuma, and B. W. Bowen. 2017. Phylogeography of lionfishes (Pterois) indicate taxonomic over splitting and hybrid origin of the invasive Pterois volitans. The Journal of heredity. Epub 2017 Jun 16

    • Posted November 27, 2017 at 2:11 am | Permalink

      I mentioned these ones on a post about a week or so ago.

  4. ThyroidPlanet
    Posted November 26, 2017 at 11:02 am | Permalink

    Sub

  5. mikeyc
    Posted November 26, 2017 at 11:05 am | Permalink

    I’m not at home so can’t check my copy of Speciation so just a brief question before reading this post in depth. You mentioned that Dr Orr and you estimate “…that producing a new species in this way in sexually-reproducing organisms takes on the order of a million years.”

    There is huge variation in reproductive cycles – some populations have several generations every year while others take several years for generations to cycle. Briefly, how is this variation reflected in the ranges in your estimate?

    • Posted November 26, 2017 at 11:21 am | Permalink

      We didn’t take into account generation times to see if there was a correlation; we just give ranges of speciation times. It’s in the last chapter.

      • mikeyc
        Posted November 26, 2017 at 11:46 am | Permalink

        Thnx

    • Kevin
      Posted November 26, 2017 at 2:45 pm | Permalink

      As I understand the Horse and Ass diverged about 4 million years ago, though their current offspring are not fertile. Technically this satisfies the requirement for speciation, though the process seems “not quite finished”.
      Similar for Lions/Tigers where the offspring are occasionally fertile (I understand only a few instances). In this case speciation is not fully completed (except perhaps for the geographical argument).

      Is this why asses are a subgenus instead of being a genus in their own right?

      Since there are several species of donkey, this raises the intriguing question as to whether certain species might actually still produce fertile offspring with horses and others not (this would indicate different points among them of speciation/subspeciation from the horse).

  6. BobTerrace
    Posted November 26, 2017 at 11:15 am | Permalink

    Subscribe

  7. Posted November 26, 2017 at 11:43 am | Permalink

    Thank you for summarizing this important piece of research. I was wondering if the generational numbers n=24, n=11, n=3 refers to the current number of descendants. If so, this species does seem to be dieing out.

  8. Randall Schenck
    Posted November 26, 2017 at 12:09 pm | Permalink

    Very glad you covered this one because I was just reading earlier today, a short article I think from Newsweek, on this from a person who had very little knowledge and left one thinking this was fast and new species and it happens all the time. A very good example of don’t believe what you read until further checking and preferably with a scientist in this field.

  9. Gregory Kusnick
    Posted November 26, 2017 at 12:48 pm | Permalink

    The male mated with another local G. fortis female, while the male mated with one of his hybrid sisters.

    I think you mean one of the four hybrid males mated with a local G. fortis female, and a different one of the four males mated with the only hybrid female. At least that’s what the diagram shows.

  10. rickflick
    Posted November 26, 2017 at 1:26 pm | Permalink

    Fascinating.

  11. Posted November 26, 2017 at 1:34 pm | Permalink

    This case was covered in quite a bit of detail in Peter and Rosemary Grant’s 40 Years of Evolution: Darwin’s Finches on Daphne Major Island (Princeton University Press, 2014), and those interested should read especially chapter 13, Speciation by Introgressive Hybridization. I’ve not yet read the new paper, but based on Jerry’s post, it seems that the new information is that the male bird which immigrated to Daphne Major, 5110, initially identified on the basis of genetic data as being a fortis X (fortis X scandens) backcross has now been identified as conirostris. In the 2014 book the Grants say that 5110’s song was unique. When reading the new paper, I’ll be interested to see if his song has been found to match that of conirostris. In 2014, they were a bit agnostic about what the descendants of 5110 should be called. There were two lines of descendants from 5110. One line, the A line, was resorbed into fortis by crossbreeding. The second, known as the B or ‘Big Bird’ line of descent, is the subject of the new paper. In discussing the latter, they mostly called it a “line of descent” or a “lineage”, but also said it was “a rare example of speciation by introgressive hybridization”. (They also record that 5110 was indeed first captured by Trevor Price, back in 1981.)

  12. Michael Fisher
    Posted November 26, 2017 at 2:35 pm | Permalink

    Am I understanding the family tree?

    Fo to F6 represents consecutive breeding seasons
    A breeding season occurs once per year

    Season F4 there were 24 birds total
    Season F5 there were a further 11 birds
    Season F6 there were only 3 further birds to add to the above totals?

    So F4 to F6 adds up to 38 living birds today [or is it 2012?} which is close to this statement which totals to 39:

    As of 2012, this inbred population has formed a closed mating group that is tiny: eight breeding pairs and 23 individuals

    It feels like I’ve misunderstood

  13. ladyatheist
    Posted November 26, 2017 at 4:44 pm | Permalink

    I have always been intrigued by the possible ways that finches have migrated from one island to another. It would have to have been a traumatic event for a little bird.

    I wonder if birds ever hitch rides on tourist boats that go to the Galapagos. That would explain this guy’s migration.

  14. Posted November 26, 2017 at 9:07 pm | Permalink

    Thanks for this. I wonder if hybrid speciation could account for what has been claimed to be sympatric speciation in Lake Victorea chichlids?

    • Posted November 29, 2017 at 12:07 am | Permalink

      On second thought, there are two things that need to be addressed.

      If the two populations can breed a hybrid, then are the two populations species or merely varieties of the same species.

      And if the two populations are species, how could they have speciated? Aslo by hybridization?
      fwer
      Sounds like the chicken and egg problem.

      One way around this is to postulate a full spectrum of inter-population fertility from say 99% fertility between organisms to 0% fertility.

      I recall and illustration of this concept by a graphic that looked like a topographic map of hills dotted about a plain. Isolated hills represented species. The big hills had little hills that represented varieties.

      We thought for a long time that beef cattle (Bos taurus) and the American buffalo (Bison bison) could not interbreed. But we now have the Beefalo, a fertile hybrid by crossing species from different genera.

      Possibly, the theoretical basis for a genuine “biological species” concept.

      How far can Patterson’s species recognition concept take us?(Patterson 1985) More recently De Queiroz (2007) Species concepts and species delimitation.

  15. Posted November 27, 2017 at 1:39 am | Permalink

    Very interesting. To a lay person such as myself the detailed mechanics of speciation is difficult to wholly comprehend. It is my misfortune however to occasionally cross paths with a creationist, who regurgitates the mantra that microevolution may exist but never macroevolution. “Who has ever really SEEN macroevolution?” is the theme. My rejoinder has to now been the existence of ring species. I will reread this post a number of times now to see if I comprehend it enough to add this to my arsenal of responses to this irritating question.

    • Posted November 27, 2017 at 2:17 am | Permalink

      PCC(E) has mentioned that there are no true ring species, in that their genetic divergence isn’t too great among neighbouring populations. All “ring species” (dare I call it “broadly construed”?) have relatively large genetic differences between at least two neighbouring populations.

  16. johnw
    Posted November 27, 2017 at 9:34 am | Permalink

    Great post. Speciation is on my list to read, we’ll see if I ever get to it. I’m almost all audiobooks these days and I’m guessing there’s no audio version.

  17. murali
    Posted November 29, 2017 at 4:58 pm | Permalink

    Too bad there is no Kindle edition of Speciation. I don’t have much space at home

    😦


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