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.

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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