Most evolutionists think that speciation, which we see as the origin of a new group whose members are unable to produce fertile hybrids with other such groups (but whose members are interfertile with each other) occurs in the following way. Populations of a single species become geographically isolated by the interposition of geographic barriers like mountains, deserts, water, continental drift, etc. These barriers can either arise de novo, like the Andes, thus isolating populations on either side of them, or result from a rare migration event that is a one-off, like the invasion of the Galápagos by ancestral iguanas, tortoises, or finches. By preventing the mixing of genes among populations of what was initially a single species, the populations can then diverge genetically, often by natural or sexual selection, but also by processes like genetic drift. Different environments, different selective pressures and different mutations will then assure that the geographically isolated populations will travel along different evolutionary pathways.

When sufficient genetic divergence has occurred that the populations can no longer produce fertile hybrids if they were once again to come into contact, we say that they are separate biological species. The genetic barriers preventing successful hybridization, called reproductive isolating barriers, are diverse: they can include a preference for different environments, mating at different times (“temporal isolation,” which occurs in corals), a dislike of mating with the other species (“sexual isolation”, very common in birds and flies) or the production of either inviable or sterile hybrids (e.g., the sterile mule) when members of different species do mate. What has happened is that the geographic isolation allows the evolution of genetic isolation up to the point of speciation. 

The scenario I just described is called allopatric speciation (from the Greek meaning “different places”). But there is evidence that species can form without such geographic isolation, especially in the case of polyploidy in plants, in which two species hybridize (or a single species doubles its genome), and genetic processes in the hybrid make it a different species from either parent. This can take only a handful of generations. And we are learning that, more often than we thought, species can still split while exchanging some of their genes.

Now all of this represents our best current take about the origin of species, which is summed up in the technical book I wrote with Allen Orr in 2004, Speciation. These views were not developed by Darwin, as he didn’t have a clear idea of the relationship between species and reproductive isolation. Although his most famous book is called On the Origin of Species, it says little about that issue, but rather deals more with the origin of adaptations within a species.

But how long does it take for this process to occur? That’s harder, as only in very rare cases can we actually observe new species arising, and only when it’s fast—as in polyploidy (about 3 generations to get a new plant species). Without our having been there, we have to use indirect methods.  Allen Orr and I, in a pair of papers in Evolution (references below), tried to do that with the fruit fly Drosophila. 

What we did was take named species of flies whose degree of reproductive isolation—only sexual isolation and hybrid inviability and sterility—had been measured in the lab, and estimated the “genetic distance” between those species using early electrophoretic data. In that way we could correlate the degree of reproductive isolation of different species with the degree of genetic divergence between them. Assuming the latter statistic accumulates roughly linearly with time (the so-called “molecular clock”), we could then get an idea of how fast reproductive isolation accumulates. Our admittedly rough estimate—for we neglected forms of reproductive isolation impossible to measure in the lab (i.e., ecological differences)—was that it took between 200,000 and 2.7 million years for one species of Drosophila to split into two. (The faster estimates are for species now found in the same area, for in such cases natural selection against hybridization, if hybrids are sterile or inviable, can speed up the evolution of reproductive isolation.)

In our book Speciation, Allen and I considered many other groups, and concluded that in general speciation takes between 0.5 and 5 million years, with some exceptions like polyploidy. But that’s a very rough guess based on many kinds of data, including fossils. That is, by the way, ample time to generate the millions of species living today, even taking pervasive extinction into account.

A new paper in PLOS Biology by Camille Roux et al. (reference and free link below) uses a related method to see how much genetic distance between groups is sufficient to make them different species, although in this case the species were designated simply by nomenclature rather than by strict consideration of reproductive isolation. The methods are complex, but I’ll oversimplify them to give the general result.

Roux et al. used data on 61 pairs of species or populations; these were diverse, including worms, fish, crustaceans, mammals, and insects. All of these pairs had extensive molecular data known for them. Ten were pairs taken from the literature, 22 were pairs of named, distinct species, and 29 were pairs of populations considered to be within the same species.

Using various complex models, the authors attempted to see how much gene flow was going on between these pairs of taxa, relating that to the genetic distance between them. (There are ways to do this without it being circular.) They used various models, including complete allopatric speciation, speciation occurring while gene flow was going on between the separating groups, and gene flow that occurred after geographically isolated groups once again came to live in the same place. What they came up with is a plot showing the relationship between the degree of genetic difference between pairs of species or populations (Da below) and the probability of ongoing gene flow between taxa (P in the diagram below).

What does this diagram show? Well, as you move along the horizontal (X) axis from left to right, the genetic distance at “neutral” sites increases, meaning that the species or population pairs get older. And you see from the Y axis (gene flow) that as the age between taxa increases, the amount of gene flow between them decreases, finally winding up at zero—at which point they are full biological species (in red). The Big Deal about the paper, however, is the fairly narrow transitional “gray zone”: the bar that marks the transition between fairly free gene flow (populations or incipient species) and full species. That gray bar extends from 0.5% to 2% sequence difference at “neutral” sites.

Surprisingly, the transition zone is about the same regardless of whether the groups are geographically isolated or not; I would have expected that geographic isolation would speed up speciation by impeding “annoying” divergence-preventing evolutionary difference. The authors were also surprised at this, but said this may be because their range data were not so great. Further, the authors recognized several new species, which looked pretty much the same but whose genetic distance put them on the right (i.e., not left) side of the speciation threshold.

The fact that diverse taxa adhere to the same “threshold” of speciation seems surprising, implying that the amount of neutral genetic difference associated with speciation is roughly the same for very different groups. From that observation the authors conclude this (my emphasis):

. . . our report of a strong and general relationship between molecular divergence and genetic isolation across a wide diversity of animals suggests that, at the genome level, speciation operates in a more or less similar fashion in distinct taxa, irrespective of biological and ecological particularities.

This conclusion is echoed by a PLOS blog post on the paper by grad student Jenns Hegg from the University of Idaho:

Does this paper tell us what is and isn’t a species? No, it doesn’t. But, it gives us an idea of how to understand the process of speciation across species. It also indicates that speciation happens (genetically at least) in pretty similar ways in all species regardless of the specifics of the population…which is good news for anyone interested in developing better ecological and evolutionary theories to explain how species come about through natural selection.

Well, both of these conclusions are dubious. Yes, it was surprising that the “gray zone” wasn’t so different among diverse taxa, but remember that these taxa are not all phylogenetically independent. Some groups are used more than once, so we can’t be sure that every data point represents an evolutionarily independent pair of taxa. Further, the sample size is limited (e.g., no Drosophila!) Also, there are these problems:

• We know of some cases of speciation that are very rapid, including about 4000 years in some cichlids, 50 years in polyploid plants, and a few hundred years in sunflowers (see here for some fast cases of speciation that are outside the gray zone). Polyploidy, or rapid ecological speciation, obviate these conclusions. One cannot conclude that all speciation events adhere to the pattern above.

• A constant genetic distance of 0.5%-2% does not necessarily mean that species take roughly the same time to evolve in nature. That’s because the molecular clock ticks at different rates in different taxa, so a divergence of 1% in flies could represent a very different time for a divergence of 1% in mammals or worms.

• We already know that different taxa speciate in different ways, so saying that “speciation happens in similar ways in all species regardless of the specifics of the population” is just wrong. (Polyploidy instantly invalidates that statement!) And it’s wrong to say, as the authors do, that “speciation operates in a more or less similar fashion in distinct taxa.” What the data show is that the neutral genetic distance associated with the reduction of gene flow is similar in this small sample of species. The paper doesn’t—and cannot—say anything about the process or “mechanism” of speciation, which we already know differs in different groups. We can’t even say that the rate of speciation is similar in different groups until we know how neutral genetic distance translates into years among different groups.

I think, then, that too much is being made of this paper, though the results are still quite interesting. But we need a much better data set, a much better calibration of the molecular clock in different groups, and some clearer thinking about what the authors mean by “speciation operating in a similar fashion.” We already know that in different groups different reproductive isolating barriers are important (pollinator isolation in orchids, sexual isolation in birds, etc.—see Speciation). And if by “similar fashion” the authors mean “similar rates,”  well, that remains to be seen as well.

The authors discuss the use of this gray-zone metric as a conservation tool—a way to distinguish taxa to put them within the regulations for protection of endangered groups—but I won’t open that can of worms.

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Coyne, J. A. and H.A. Orr.  1989.  Patterns of speciation in Drosophila.  Evolution 43: 362-381.

Coyne, J. A., and H. A. Orr. 1997. “Patterns of speciation in Drosophila” revisited. Evolution 51:295-303.

Roux C, Fraïsse C, Romiguier J, Anciaux Y, Galtier N, et al. (2016) Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLOS Biology 14(12): e2000234. doi: 10.1371/journal.pbio.2000234

Yesterday I gave the background necessary for understanding a new paper in Evolution by Christopher H. Martin et al. (reference and link below). Today I’ll briefly describe the paper’s findings—findings that cast doubt on one of our premier examples of sympatric speciation.

That example was the existence of assemblages of cichlid fish in small volcanic crater lakes in Cameroon. Because genetic evidence by Schliewen et al. (1994) showed that each assemblage was monophyletic, that is, appeared to descend from a single common ancestral species that invaded the crater lakes some time ago (between 1 and 2.5 myr for Lake Barombi Mbo and 100,000 to 2.5 myr for Lake Bermin), this gave evidence that the formation of 11 species in Barombi Mbo and 9 in Bermin had occurred sympatrically—without geographic isolation of populations.

Read yesterday’s post for background. Here are the two radiations at issue, showing the location of the crater lakes.

The authors re-did the genetic analysis of the two radiations shown above (and others from different lakes as well), producing more than 350 million DNA sequences. (This is the level of analysis that new techniques permit us.) From this they then re-did the phylogenetic analysis. Here’s what they found.

• The “monophyly” (descent from a common ancestor) of the two radiations shown above is weaker than previously thought. The authors conclude that this monophyly, which is crucial evidence for sympatric speciation, is not “strongly supported.”

• Further, there appears to have been substantial introgression (movement of genes) between not only some of the species in each of the two radiations, but also between the species in the lake and different “outgroup” species in rivers outside the lakes. This suggests that there have been multiple invasions of the lakes by ancestors of the crater-lake fish, and this again militates against a single common ancestor forming multiple species in the lake.

How did Martin et al. detect this introgression? By looking at the asymmetry of genetic similarity between species within the radiations, and also between those species and others outside the lake. As they explain:

Information about the directionality of introgression comes from the asymmetries in the relationships among populations given the tree. For example, if we imagine a tree ((A,B)(C,D)) with subsequent introgression from B into C, population C would show unusually high covariance with A, but B would not with D.

In other words, if the tree shows two sister pairs of species (species A closely related to B, and species C closely related to D, and the (A + B) group more distantly related to the (C + D) group, gene movement between B and C, which reside in different groups, could be detected when some genes in C could also be found in A. This shows a resemblance between species of different groups not seen in the species B and D, also residing in different groups. This pattern could only occur if there was movement of genes between species in different groups, either before or during speciation.

I won’t go into the gory details, and, truth be told, the complete details of the methodology elude me, but the results are clear: the species in the lakes are not convincingly monophyletic, and also exchanged genes not only with each other, but with some species outside the lake.

How could this happen? In several ways, all of which violate the notion that speciation (the generation of largely reproductively isolated entities within the lake after an invasion by a single ancestor) occurred with free gene flow. First, there could be multiple invasions of the crater by fish from a single lineage, with that lineage changing genetically between invasions.  That could mean that some reproductive isolation could have evolved between the invasions, and that could promote speciation between the fish in the lake.

That reproductive isolation wouldn’t be complete, and the incipient species could exchange genes but gradually become full species due to the process of reinforcement. In this process, species that already have evolved some reproductive isolation—in the from of hybrid problems like hybrid sterility or inviability—then experience natural selection for increased sexual isolation, because those individuals in each incipient species that mated with their own kind would leave more genes than those which mate with the other kind. This could eventually lead to reproductive isolation, but also to the misleading appearance of monophyly among species due to gene exchange. This is not sympatric speciation because a period of geographic isolation would be necessary to evolve the “reproductive isolation” genes.

An alternative scenario involves multiple colonizations of the lake by either different ancestral species or, as above, different segments of a single ancestral lineage at different times. The multiple colonists could then form a hybrid swarm, with copious mixing of genes, and then that swarm could sort itself out into different species in the crater lake. Again, some allopatry is required.

In both cases, the gene exchange that occurred while new species were forming in the lake gives them the appearance of all descending from a single ancestor that invaded only once, but in reality the speciation involved an allopatric (geographically isolated) phase.

Whatever happened, the signal of gene exchange is clear, and pretty much eliminates these two crater-lake radiations as a result of purely sympatric speciation. (I hasten to add that some of the genetic divergence between species surely evolved within the crater, but the reproductive isolation also required an allopatric phase for at least part of the process.)

The authors note too that the crater lakes do have some different ecological niches, and, if fish tend to mate where they live, that would facilitate speciation within a small area, but an area in which there is still some spatial isolation between the speciating populations. Traits in animals or plants that produce an automatic association between location and time of mating are called “magic traits” because they have a double effect. For example, a single pregnant female fish might like to hang around at the bottom of the crater lake, and if its offspring are produced there, and they show a tendency to stay there, as well as mating with others that are nearby, this would lead to a kind of geographic isolation based on restriction of gene flow between fish that like to live in other parts of the lake. All that is required is that fish tend to mate and produce offspring in certain areas, and offspring mate with those nearby. This would eventually yield selection to adapt to your habitat, and the appearance of reproductive isolation as a byproduct. In support of this, the authors note that many of the species in the two radiations above are “habitat specialists”, found most often in one particular part of the lake.

So the existence of “magic traits” can facilitate sympatric speciation, but that’s not sympatric speciation in its strictest sense, which involves the generation of new species without any physical separation. The authors conclude:

Available evidence suggests that all crater lake cichlid radiations speciated with the help of double invasions (Schliewen et al. 2006; Geiger et al. 2013) or remain stalled as incipient species complexes (Elmer et al. 2010b; Martin 2012, 2013). To our knowledge, all compelling examples of sympatric speciation besides crater lake cichlid radiations involve some form of au- tomatic linkage between ecological divergence and mating time or location, known as “automatic magic traits” (see review in Servedio et al. 2011).

What are those compelling examples of sympatric speciation beyond the crater lake cichlids? One of them are the two sister species of palm trees that diverged on Lord Howe Island. (See my review of this situation in my News and Views “Speciation in a small space“; reference below).  In that case, a few palms from a colonizing species found themselves in dry soil, which automatically makes them flower earlier than plants on wetter soil (in dry soil you must to get your seeds out ASAP because soil drying over time can reduce your ability to reproduce). Thus those palms, producing pollen and ovules at the same time, were more likely to mate with each other than with their conspecific palms on wetter soils that flowered later. This could eventually produce differential adaptive evolution and reproductive isolation. Living on dry soils is one example of a magic trait in which habitat and reproduction are automatically associated.

Martin et al. cite three other examples of sympatric speciation that they consider convincing. One is the case of two groups of pea aphids that live on alfalfa and tomato in the U.S., and are said to have speciated in sympatry (tomato fields often lie next to alfalfa ones). But Allen Orr and I showed in Speciation that this is not a good case of sympatric speciation, since the divergence probably occurred in Europe, where the aphids live on multiple plants, and was probably followed by double colonization of the U.S.

The other two cases involve mole rats and spiny mice in Evolution Canyon, a canyon in Israel with ecologically distinct sides. I haven’t yet read those papers, so I can’t comment on them. But what’s clear is that, after the Martin et al. paper, perhaps the most convincing example of speciation we had is no longer so convincing.

What remains? The Lord Howe plants are a good case of speciation on a very small island, but need further investigation to see if “magic traits” could have been involved. Besides those plants, there are a few other cases (other fish and fig wasps) we mentioned in Speciation, but the evidence is not very strong.  All the data to date suggest that while sympatric speciation with free gene flow is a theoretical possibility, there is little evidence for it occurring in nature. There are certainly some cases (everything possible happens at least once in evolution), and of course getting good evidence for those cases would be hard. What we can say, though, is that there are not enough data to support the frequent assertion that sympatric speciation is common.
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Coyne, J. A. Speciation in a small space. Proc. Nat. Acad. Sci. USA 108:12975-12976.

Martin, C. H., et al. (2015). Complex histories of repeated gene flow in Cameroon crater lake cichlids cast doubt on one of the clearest examples of sympatric speciation. Evolution 69(6): 1406-1422.

Schliewen, U. K., et al. (1994). Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368: 629-632.

I will break up my discussion of the paper below into two parts that will appear today and tomorrow. This is because I want to avoid a single long post that may put off readers. I give references to all the papers mentioned at the bottom of the post.

All evolutionists agree, and the data show, that nearly all new species form as descendants of what were populations of a single ancestral species. (Occasionally new species, especially in plants, form after hybridization of two pre-existing species.) One of the biggest controversies in my own field of speciation is this: can new species form in one area without any geographic isolation of populations (“sympatric speciation”), or is a period of partial or full geographic geographic isolation necessary (“parapatric” or “allopatric” speciation, respectively)? (I’ve simplified the meaning of these terms a bit.) While theory shows that geographic isolation facilitates the development of reproductive isolating barriers between populations (sexual isolation, hybrid sterility, and so on) that are the sine qua non of speciation for most biologists, some theory also suggests that geographic isolation is not necessary: under special conditions, new species can form in one area in situ.

The data, summarized in my book Speciation with Allen Orr (now a decade old), suggest that geographic isolation is usually necessary, but there are a few cases implying speciation without any geographic isolation. These are hard to demonstrate unequivocally, largely because closely related species that now live in the same area could have speciated in allopatry (different areas), and then come into secondary contact after the reproductive barriers evolved in isolation. Since it’s harder to form species sympatrically, to demonstrate this process one must rule out that ancestral populations were ever isolated geographically. Since that’s hard to do (speciation takes thousands to millions of years to complete), convincing cases are rare.

In Speciation (pp. 142-143), Allen and I laid out criteria for showing convincing cases of sympatric speciation. They include the presence of sister species (each other’s closest relatives) in the same area; the demonstration that these are indeed “good” species (i.e., they are distinct groups that never or rarely exchange genes); the demonstration that their status as each other’s closest relatives does not come from hybridization between more distantly-related species (this would homogenize their genomes and make them look closely related when they really aren’t); and the hardest bit: showing that these those sisters species descend from populations that were never geographically separated. That’s the biggest issue, because when you see two closely related species living in the same area, how can you convincingly show that their ancestors always lived in the same area?

Allen and I decided that one of the best situations for meeting these criteria occur on islands: either oceanic islands (islands like Lord Howe or St. Helena that were formed without life on them, usually as volcanoes that rose above the sea), or “habitat islands”: isolated patches of habitat that have existed for a long time. (Landlocked lakes are one example.) If you could show, for instance, that on one such island you find two or more sister species that do not occur elsewhere (i.e., are endemic to that island), then that would be pretty strong evidence that those species had formed sympatrically on the island, descending from a common ancestor that invaded the area long ago.

Trevor Price and I tested this theory by looking for endemic sister species of birds on oceanic islands.  In a paper published in Evolution in 2000, we found not a single such case on 46 isolated oceanic islands, implying that sympatric speciation was rare in birds. (If it didn’t occur on islands, it is unlikely to occur on continents.) Further work by Yael Kissel and Tim Barraclough in 2010 showed the same situation in several other groups, including lizards, mammals, and flowering plants. Sister species on islands were observed only when the islands were so large that geographic barriers were likely to have been present. This further implies that sympatric speciation is rare, at least in those groups studied.

In contrast, though, work by Papadopulos et al. on the flora of Lord Howe Island (a small oceanic island between Australia and New Zealand, with an area of about 15 square kilometers) shows the existence of sister species in about nine groups of plants, most notably two species of endemic palm trees that are wind pollinated. Since the sister species in these groups are found nowhere else, they likely formed on the island. This, too, seems a pretty good case of sympatric speciation.

But in vertebrates we have only a couple of cases—all involving fish—that point to sympatric speciation. These cases involve species living in small lakes that fill the craters of extinct volcanoes—”crater lakes”.  In 1994, Ulrich Schliewen and his colleagues described groups of closely related cichlid species, each group descending from a single common ancestor, that inhabited crater lakes in Cameroon. (Such cases have since been described in lakes in Nicaragua as well). Lake Barombi Mbo, only 2.3 km across, contains a group of 11 “monophyletic” cichlid species (descended from a single invader), while Lake Bermin, only 0.7 km across, has a monophyletic group of 9 cichlids. Here are the two lakes:

And here are the putatively monophyletic species flocks, shown in the paper of Martin et al. mentioned below. (There are only 10 species shown for Lake Barombi Mbo because the authors sampled only 10 of the 11 for genetic markers.)

Because the lakes are no longer connected to rivers that could carry in fish (lake Bermin has an outflow but no inflow); because they are small and uniform (so that raising or lowering the lake levels would not create isolated pools that could facilitate allopatric speciation); and because each small lake harbors a group of species from one putative invading ancestral species, this situation fulfills all four criteria we proposed for sympatric speciation. When we wrote our book, Allen and I considered this perhaps the best case of sympatric speciation in nature.

But that’s now in question. A new paper in Evolution by Christopher H. Martin et al. (reference and link below) genetically examined the radiations in these lakes and finds that sympatric speciation isn’t that likely after all. Today I gave you the background; tomorrow I’ll show you the results.

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Coyne, J. A. and H. A. Orr (2004). Speciation. Sunderland, MA, Sinauer Associates.

Coyne, J. A. and T. D. Price (2000). Little evidence for sympatric speciation in island birds. Evolution 54(6): 2166-2171.

Kisel, Y. and T. G. Barraclough (2009). Speciation has a spatial scale that depends on levels of gene flow. Amer. Natur. 175: 316-334.

Martin, C. H., et al. (2015). Complex histories of repeated gene flow in Cameroon crater lake cichlids cast doubt on one of the clearest examples of sympatric speciation. Evolution 69(6): 1406-1422.

Papadopulos, A. S., et al. (2011). Speciation with gene flow on Lord Howe Island. Proc Natl Acad Sci U S A 108(32): 13188-13193.

Schliewen, U. K., et al. (1994). Sympatric speciation suggested by monophyly of crater lake cichlids. Nature 368: 629-632.