The Biological Species Concept, or “BSC,” was devised and refined by evolutionist Ernst Mayr in the 1930s and 1940s as a way to conceptualize the distinct groups—”species”—that we see in most plants and animals. It runs as follows (in my words), which also includes how we conceptualize different biological species.

A biological species consists of a group of populations that, where they coexist in nature, exchange genes through reproduction. Two populations that coexist in one area but do not exchange genes are considered members of different biological species. 

One of the advantages of the BSC is that it enables us to immediately solve the species problem that eluded Darwin: why is nature divided up into distinct clusters rather than existing as a continuum, clusters most visible where they coexist?  Under the BSC, the problem of the “origin of species” simply becomes the problem of “the origin of those barriers that prevent interbreeding”—and that is a tractable problem.  Again, see Coyne and Orr for our best take on how these clusters form.

Of course there are problems with this concept (it’s not an a priori definition, but an attempt to conceptualize in words what we see in nature). These problems include judging populations that live in different areas like islands of an archipelago, how we deal with groups that hybridize just a little where they coexist, and, most important for this article, what we do with species that are asexual, lacking the possibility of exchanging genes. We discuss all these issues in the first chapter of my book Speciation (2009) written with Allen Orr, but one issue we didn’t resolve properly was that of asexual organisms.

So what about those pesky “asexual” organisms? How can we conceptualize species in groups like bacteria? Well, the first thing we need to determine is whether they form distinguishable clusters like birds or turtles. If they don’t, then there’s no need to conceptualize nonexistent clumps. In our 2009 book, we reviewed the literature, which was scant at that time, and decided that the evidence was mixed about whether bacteria (considered asexual) formed species, but there are surely some clumps among them. So we restricted the rest of the book to sexually-reproducing organisms. Still, bacterial “species” are given names, like E. coli, but do all bacteria considered E. coli really comprise members of a distinct cluster? If so, how?

The literature has expanded since then, and the paper below, which I’d missed and which is now seven years old, makes a pretty good case that in bacteria, at least, there are species, and, more important, they are conceptualized in a way similar to that of the BSC. In other words, there are bacterial clusters, and each cluster is characterized by its ability to exchange genes among individuals. Members of different clusters, however, don’t exchange genes. In other words, bacteria do consist largely of genetically isolated clusters. The authors, though examining only bacteria (there are other asexually reproducing organisms, like bdelloid rotifers), conclude that life in general conforms to the BSC. That’s a bit too expansive a conclusion (see the title!), but their results for bacteria seem good.

Click to read, or see the pdf here.

The key to this paper is recognizing that bacteria are not in fact completely asexual, though they often reproduce that way. But they also have a form of sex in which genomes of two different individuals can sidle up to each other and recombine to produce new genes. This process, called homologous recombination, occurs via cell-to-cell contact or transfer of DNA through tubes (“pili”) connecting different individuals. This process is called conjugation.

Here’s a photo from Wikipedia showing two bacterial cells moving DNA through pili:

This movement is one-way: the DNA (a single chromosome with double-stranded DNA) from one individual moves to the other. After that, there can occur a form of “sexual” reproduction in which different copies of the same gene can line up and recombine, producing a new gene. A similar process happens during meiosis (gamete formation) in sexually-reproducing organisms.

In bacteria this mixing-up between similar genes is called homologous recombination because it changes the composition of a gene by recombining its DNA with the DNA from a similar gene in another bacterium.  There are other forms of DNA exchange in bacteria in which a bit of DNA or a “plasmid” from one individual simply inserts itself somewhere else in the genome of another individual, but this is not recombination in the traditional sense, for it doesn’t involve two different copies of the same gene recombining to form a new gene.  The paper by Bobay and Ochman deals with homologous recombination,

Their method of determining whether two individuals in a named bacterial species can recombine their DNA in this way is complicated, and I’d best leave it for the experts here. But I will say that it involves showing that individuals in a group share the same variants in a given gene segment (10,000 bases were sequenced) as do other individuals in a group. For example, in one ten-base stretch of DNA, an individual may have  GTTACTCTAA, another would have GTTAGTCTAA, and another GTTACTCTAC, and still another GTTACTAC, representing combinations of DNA bases that could occur by recombination.

If you see this pattern among individuals of a named bacterial species, that’s indicative that homologous recombination—bacterial “sex”—is going on. This form of recombination is called “homoplasic” recombination because the variants all come via mutation from a single original genome present in the individual that founded the species.

One alternative is that we are dealing with two related species in which similar DNA sequences only look as if they’ve undergone homologous recombination because two groups shared a common ancestor and then the descendants had similar (“convergent”) mutations. This, called  “nonhomoplasic recombination”, is not caused by genetic exchange.

The authors have ways to distinguish these two types of recombination, and devise a ratio they call “h/m”, showing the ratio of the degree of homoplasic recombination (true sex) from nonhomoplasic recombination (independent mutations in different groups that superficially mimic sex).  The higher the h/m ratio, the more sex individuals in that group are having.

The authors calculated h/m ratios for 91 named bacterial “species”, using, of course, a large number of genomes sequences for each species, because one needs to survey the variation among individuals in that 10,000-base segment. (They also did simulations to verify that they could tell “h” from “m”.)  It turns out that over half of the 91 named bacterial species they examined conformed to biological species in which there was evidence of “h” recombination among individuals. Here’s one below, in which the h/m ratio increases. reaching an asymptote, as they looked at more strains. (This increases your power of detecting shared variants). 54 of the 91 named bacterial species looked like this, so the BSC holds for at least half of named bacterial species, and the authors sampled widely in bacteria.

A biological species in bacteria:

Here’s what was thought to be one species but, when they added more strains, they saw two clusters, one that behaved as like the one above, but the other, relative to the other group, showed very low h/m ratios, indicating that the two groups didn’t have homologous recombination between them. That is, they were different “biological species”. When they took out the low h/m group, B. pseudomallei behaved nicely. Here, then, we have two species that were given the same name, perhaps because they had similar morphologies or culturing requirements, or because the genetic distance between them (indicating the time of separation) was pretty low, suggesting a recent origin. These “cryptic species” were seen in 21 of the 91 named bacterial species.

Two biological species in bacteria that went under one name:

And the third group by itself had low h/m ratios no matter how many strains they included, so that there was no ability to assess gene flow at all—perhaps because these species simply don’t undergo any homologous recombination. Here’s one:

Thus 73/91 groups tested showed patterns consistent with a reproductive-isolation based species concept.

To test that their method did indeed detect groups analogous to biological species in more familiar animals, the authors did the same kind of h/m test for two pairs of related but clearly distinct biological species; one was the related species Drosophila melanogaster and D. simulans, and the other Homo sapiens and the chimp Pan troglodytes. As you see below, they were able to detect reproductive isolation between the group using a similar 10,000 base-pair fragment. (In all cases they looked at many replicates of the species on the left and a single sequence for the species on the right, which is why the “other” species forms a straight line: we have one sequence compared to many sequences in the other species, and all comparisons show a low h/m ratio.)

Humans vs. chimps, also good biological species:

The conclusion, then, is that the BSC is pretty good in conceptualizing species in bacteria: there are groups that exchange gene segments, and other groups (different “species”) that do not exchange DNA via homologous recombination. Remember: all of this was judged from looking at DNA sequences, not seeing gene exchange directly.

The big conclusion (from the paper):

That species can be universally defined based on gene flow implies that many of the same factors are operating in the process of speciation across all lifeforms. Differences in genomic properties (such as ploidy, recombination frequencies, and reproduction, and rates of gene acquisition) and demographic parameters (such as population sizes, geographic distribution, and rates of migration) will impact the pace at which microbes speciate relative to sexual organisms. However, the application of a single genomic-based BSC criterion to delineate species makes it possible to define species and study speciation under a similar framework across the tree of life.

Well, they need to look at other putatively asexual groups to see if this method also shows the existence of interbreeding groups reproductively isolated from other such groups, but at least for bacteria we see that many of them form clusters.  Two questions remain:

1.) What is “speciation” in bacteria, then?  One of the paper’s most intriguing results is that if you take pairs of bacterial “species”, the degree of reproductive isolation between them isn’t positively correlated with the time separating them, as judged by the “genetic distance”, or whole-genome divergence, between them. This is hard to understand because it implies that, unlike sexually reproducing organisms like fruit flies and mammals, reproductive barriers don’t form as a simple byproduct of the time of divergence from their common ancestor. This is the case because in those groups reproductive barriers are usually byproduct of divergence between populations by natural selection and genetic drift, which drive species apart genetically as time passes.

Why isn’t this the case in bacteria? I have no idea! My only suggestion is that “species formation” might be so quick in bacteria that you simply don’t get a correlation of time with reproductive isolation. That would imply that it’s virtually instantaneous.

2.) Why do bacteria form clusters?  In more familiar animals, clusters arise because after reproductive barriers arise, an interbreeding group is free to adapt to its environment without “pollution” from other species that would efface the clusters. The genetic divergence is reflected in not just reproductive isolation, but in the way organisms look or behave.  This may also be true in bacteria: each cluster might represent a group adapted to a particular ecological niche.  This would be hard to test for naturally-occurring bacteria, but might be tested in pathogenic bacteria, whose habitat (us) is more easily studied. As I recall, each bacterial species does its own thing in its own way, but that’s not really an answer to the question.

A final note: this paper was difficult, and I may have made some errors in summarizing its results. (I could read it only twice before I had to write about it here.) Perhaps the authors will read my summary and correct any mistakes.

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Reference: Bobay LM, Ochman H. Biological species are universal across Life’s domains. Genome Biol Evol. 2017 Feb 10;9(3):491–501. doi: 10.1093/gbe/evx026.

By Jerry Coyne and Greg Mayer

Yesterday Carl Zimmer wrote a piece for the NYT on species concepts and conservation. Both Greg and I, who discussed the piece and are coauthoring our take on it, found that while Zimmer does not take a position on species concepts (which is good thing), it does have a theme.  And the theme seems to be this: that conserving biological diversity depends critically on what biologists decide a “species” is.  Now this argument is not, in our view, correct, because you can conserve biological diversity regardless of your species concept, even though some biologists seem to feel that we must be conserving species.  If you take that latter point of view, which we see as misguided, then you’re screwed, as there are, as Zimmer notes, dozens of species concepts, and each will lead you to a different decision about populations of an animal or plant. Is a population of owls long isolated on an island a different species from its relatives? That is largely a subjective judgment.

Click to read:

As Jerry emphasizes in WEIT, the species concept one uses depends on what question one is asking. To evolutionists, the main question about the diversity of nature is this: “Why is it lumpy?”  That is, why do animals and plants appear not as a continuum, but in pretty discrete groups.  Look at the birds out your window and see if you have any problem telling which is which. And so it is with most animals and plants—so long as they live in the same place, i.e., are “sympatric”. (For populations that are not sympatric, but live in different areas—i.e., “allopatric”—problems arise. and these are the problems that Zimmer describes in his piece.

At any rate, the explanation for the lumpiness in one area began to be solved when biologists adopted what we call the “biological species concept”, or BSC, devised by several biologists in the 1930s, notably Ernst Mayr. (Zimmer describes him as a “German ornithologist” but he really was a German-American evolutionist—the “Darwin of the 20th century”—who held forth on far more things than birds.) The BSC is basically this:

Two populations are members of different species if they live in the same area in nature but do not produce fertile hybrids in that area.

That is, they do not exchange genes because of what we call “reproductive isolating barriers” (RIBs) that prevent genetic interchange. These barriers keep populations distinct, and allow them to undergo evolutionary divergence without being held back by gene flow.  It is this feature—reproductive isolation—that leads to nature’s lumpiness, and it is the origin of these barriers that explains, to an evolutionist, the origin of species.

It turns out that these barriers usually form when populations evolve in different places. Then, when the evolutionary divergence has proceeded to the extent that there is reproductive isolation between the populations when they come back together in sympatry, we now have evolved two species from a single ancestor.  RIBs come in many forms: hybrid inviability, hybrid sterility (the mule), ecological isolation (related species prefer to live in different sub-areas of the environment, or are confined there, and thus do not meet), temporal isolation, so that populations mate at different times (common in marine organisms), and differences in mate preference, so members of each species prefer to mate with individuals of their own “kind,” forming substantial barriers to gene flow.

If we can understand how one ancestral species forms two populations that cannot exchange genes, then we’ve solved the problem of the origin of species—a problem that, despite the title of his great book, Darwin didn’t come close to resolving.   Now most evolutionists realize that the answer is the origin of RIBs. In fact, neither of us have ever found a scientific paper on how species form that doesn’t involve the origin of RIBs: a tacit but telling admission that the BSC is the answer to most questions about speciation.

The problems that Zimmer outlines largely involve animal populations that are geographically isolated from one another, so the BSC can’t really be applied: the populations don’t coexist. Some of them, like the giraffe populations, breed with each other like gangbusters in zoos, but that’s a very weak test of conspecificity, because some species that live in the same area without interbreeding have their RIBs broken down in captivity (this is true of many fruit flies and of species isolated by ecological preferences). One thing we can say is that if two populations in captivity produce hybrids, but that those hybrids are inviable or sterile, then, yes, they are members of different species. But breeding in captivity, something usually impossible to test, is at best a one-way test.

In 2016, Jerry wrote about the giraffes here: the populations, which look different, live in complete geographic isolation, but breed like crazy in zoos, producing viable and fertile offspring.  What do we call them? We don’t know, but we’d say that they’re subspecies rather than full species. It’s a judgment call. The non-BSC people have simply raised the rank of all the traditional giraffe subspecies to species. Nothing prevents people from wanting to conserve subspecies– we sure do! People tried desperately to conserve the two subspecies of white rhinos, well before it became fashionable to raise the subspecies to species.

In recent years, Christophe Dufresnes, a herpetologist at Nanjing Forestry University in China, has used this concept to classify different species of frogs in Europe.

Some of the groups of frogs interbred a lot, whereas others had no hybrids at all. By analyzing their DNA, Dr. Dufresnes found that groups with a recent ancestor — that is, those that were more closely related — readily produced hybrids. He estimates that it takes about six million years of diverging evolution for two groups of frogs to become unable to interbreed — in other words, to become two distinct species.

“This is very cool,” Dr. Dufresnes said. “Now we know what the threshold is to deem them species or not.”’

Well, Dufresnes is still using a proxy for the BSC, but his concept of conspecificity: the “ready production of hybrids”, is a bit off. In fruit flies, species can readily produce fertile hybrids in vials in the lab yet they don’t do so in nature. Still, Dufresnes’ approach is better than just judging by genetic distance alone, or, worse, by the degree of morphological difference between isolated populations, which may be the worst way to make a species call.

Zimmer describes the intriguing finding that polar bears and brown bears have had several episodes of genetic exchange over the last 120,000 years even though they split from a common ancestor about half a million years ago.  What do we call them? Our view is that they are biological species that have had their ecological isolation (polar bears “prefer” to live in colder habitats) broken down several times by climate change. The fact that there is historical gene exchange doesn’t mean that reproductive barriers don’t exist, for speciation can be either fully or partly reversible if RIBs change—in this case by changes in ecological isolation caused by climate change.

But our point is that we don’t have to make a a strict call about whether brown bears and polar bears are different species before we can decide whether to protect them as separate entities, or only protect one of them. Conservation decisions shouldn’t rest heavily on a particular species definition; rather, we have to decide exactly what we want to conserve: nature’s lumps (biological species), geographically isolated populations of a single species, like the giraffes, or even just populations of a single species that differ by one or a few traits, like color. As Zimmer quotes: