Why Evolution is True is a blog written by Jerry Coyne, centered on evolution and biology but also dealing with diverse topics like politics, culture, and cats.
UPDATE: Science has now corrected its post by issuing the addendum below. As you’ll see in the comments below, author Alex Fox credits this post for the correction, which is gentlemanly of him. Thanks to reader Barry for the spot.
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It is a truth universally acknowledged that the two most prestigious science journals in the world are Science, published in the U.S., and Nature, published in England. One would think, then, that their science reporting would be more accurate than the slipshod stuff you see in the science pages of the major media (the NYT is an exception). But Science slipped up this time when reporting on the independent evolution of flightlessness on the island of Aldabra twice: in an ancient white-throated rail that colonized the island and went extinct when sea levels rose, and then in more modern times (i.e., several hundred thousand years ago) when birds from the same flying lineage colonized Aldabra again and once again evolved flightlessness. (Islands lack predators and so flying, which is metabolically expensive, can often be dispensed with to gain other advantages.)
A few days ago I wrote about how nearly all the major media—tabloids and respectable papers alike—mis-reported this finding, saying that the two flightless rails were really the same species, one that had been “resurrected” or “had come back from the dead.” In reality, the three white throated rails (Dryolimnas cuvieri) are designated as subspecies, so even that reporting is wrong. But that’s minor compared to the repeated claim (see my earlier post for screenshots of the distorted headlines) that the very same species had evolved twice.
This was a big boo-boo because calling the modern flightless rail and its extinct flightless analogue members of “the same species” depended only on the similarity of two bones: a wing bone and a leg bone. There was no other fossil evidence, of course, about what the extinct rail looked like, how it behaved, or anything about the rest of its skeleton, its habits, its DNA, or its physiology. It’s simply a misleading whopper to assert that the “same species” evolved twice.
Further, the species concept used by nearly all evolutionary biologists deems two individuals members of the same species if, where they meet in nature, they can mate and produce fertile offspring. It’s a concept based on reproductive compatibility and incompatibility. Doing such a test is not possible in this case because the extinct species never had a chance to cohabit with the modern species. Just as we can’t say whether modern Homo sapiens are members of the same biological species as Homo erectus (note that they’re even given different names, but that’s based on physical differences), so we can’t say whether the ancient and modern flightless rails are members of the same biological species—much less subspecies.
As someone who spent his whole career working on speciation, including species concepts, I was thus disheartened to see this news report in the journal Science:
Note that while the report does call this “iterative evolution” (“convergent evolution” would be clearer to evolutionists), and notes the independent evolution of flightlessness, it also passes on Gizmodo’s report that evolution had “resurrected the lost species.”
Nope, that’s not true. We know nothing about the genetics, morphology, behavior, and physiology of the extinct species compared to the new one. Science had no business talking about “resurrection”, but it did.
Of course only a petulant evolutionary biologist who works on speciation would single out this error. But it’s pretty bad when one of the world’s best science journals makes a totally unwarranted claim like this.
I noticed that there’s a new book out by Peter Ward, a biology professor at the University of Washington who’s done a lot of work on nautilus cepalopods. (He’s also written several trade books in biology.) Here’s his new book, and, as you can see, the cover touts epigenetics as “Lamarck’s Revenge” (Jean-Baptiste Lamarck [1744-1829] was a French naturalist who proposed a theory of the inheritance of acquired characteristics.) The cover also promises to show how epigenetics is revolutionizing our understanding of evolution. Click on the screenshot to go to the Amazon site:
Ward references the classic study showing how starvation impacted one and perhaps two generations in the Netherlands following a WWII-era famine, but provides little hard evidence beyond that example. [JAC: see below for a discussion how even the famine study is flawed.] Without a proposed mechanism for such long-lasting effects and without data indicating such effects exist, Ward leaves readers with little more than suppositions.
And that’s the problem with the Lamarckian/evolutionary/revolutionary hypothesis. Environmentally induced changes to the DNA, usually produced by the placement of small methyl groups on DNA that affect what it does, are almost never inherited beyond one or two generations. This lack of stable change means that such environmental modifications cannot form the basis of permanent evolutionary adaptation. Ergo, it can’t revolutionize our view of evolution. As the prescient Publisher’s Weekly reviewer noted, there’s just no evidence for the heritability of “Lamarckian” changes to the DNA.
I haven’t yet read Ward’s book, and don’t want to judge it by its cover, but the Nautilus site (the name is a coincidence, and that site was funded by Templeton) has reproduced an excerpt from Ward’s book, which is the article below on “fewer species”. Click on the screenshot to read it. And it gives me no confidence that Ward’s book presents a balanced view of epigenetics.
Lamarck’s Revenge, like David Quammen’s new book on phylogeny, seems to fall into the “Darwin was wrong” genre. (Darwin was supposedly wrong because modern evolutionary theory proposes that either mutations or genes transferred from other organisms are the variational basis for permanent adaptive change, and that the environment cannot itself influence DNA sequences in a permanent way. If environmental methylation did produce gene changes that could be both inherited and adaptive, and so spread through species, it would be a major change in how we view evolution.)
I should add that Darwin himself was “Lamarckian” because he thought the environment could somehow permanently modify heredity, and, as Matthew Cobb reminded me, Lamarck thought the changes occurred not through the environment, but through the animal’s “will.” Both men were wrong about heredity, but, as Matthew suggested, Ward’s book might better be called Darwin’s Revenge! After all, Darwin’s ideas were closer to these misguided epigenetic ideas than were Lamark’s theories.
Click and read:
Now the title doesn’t say much about Lamarck or the “evolution revolution”, but the article itself does. The title itself refers to work that Ward did with his colleagues on two species of Nautilus. One species, N. pompilius, occurs widely across the Pacific, while the closely related species N. stenomphalus is found only on the Great Barrier Reef. They were distinguished as different species by differences in morphology: they differ in whether they have a hole through the center of their shell, as well as showing big differences in both internal and external anatomy.
Ward, however says that they aren’t separate species because their DNA was identical using DNA-sequencing analysis (my emphasis):
We caught 30 nautiluses over nine days, snipped off a one-millimeter-long tip of one of each nautilus’ 90 tentacles, and returned all back to their habitats alive (if cranky). All the samples were later analyzed in the large machines that read DNA sequences, and to our complete surprise we found that the DNA of N. pompilius and the morphologically different N. stenomphalus was identical. No genetic difference, yet radically different morphology. The best way to interpret this is to go back to one of the most useful analogies in evolution: of a ball rolling down a slope composed of many gullies. Which gully the ball rolls down (corresponding to the ultimate anatomy or “phenotype” of the grown animal) is controlled by the direction of the push of the ball. In evolution, the ultimate morphological fate of an organism is caused by some aspect of the environment the organism is exposed to early in life—or, in the case of the nautiluses, while they slowly develop in their large egg over the course of an entire year before hatching. Perhaps it is a difference in temperature. Perhaps it is forces that the embryo encounters prehatching, or when newly hatched, the small nautiluses (one inch in diameter, with eight complete chambers) find different food, or perhaps they are attacked and survive, i.e., have two different kinds of predators. That’s why N. pompilius and N. stenomphalus are not two species. They are a single species with epigenetic forces leading to the radically different shell and soft parts. Increasingly it appears that perhaps there are fewer, not more, species on Earth than science has defined.
Well, the differences might not be genetic, but they might not be epigenetic either: the environment could simply change the development of the organism in different places without methylating or modifying its DNA in a heritable way, just as a plant given lots of fertilizer in one plot will grow taller than a plant grown without fertilizer in another plot. There’s no indication here that the differences in morphology of the two Nautilus species are caused by methylation of the DNA or histones, or by small RNA molecules—the three ways Ward says the environment might modify genes in a permanent way.
More important, when I looked up the paper on which this statement was based, I found, contrary to what Ward implied, they didn’t look at a lot of DNA in the two species, finding it identical. The paper (click on screenshot below), published in 2016, looks at only two genes in the mitochondria, and none from the nucleus:
An excerpt from the paper above:
Here, we report the genetic analysis of mitochondrial genes cytochrome c oxidase I (COI) and 16S rDNA, commonly utilized genetic tools for the phylogeographical studies of marine invertebrates, including cephalopods (Anderson 2000; Anderson et al. 2007; Dai et al. 2012; Sales et al. 2013a) from individuals across the known locations of Nautilus populations (Philippines, Fiji, American Samoa, Vanuatu, and eastern Australia – Great Barrier Reef). We chose COI and 16S because of their variability and success in past studies, and to align with sequences generated for this study with previous nautilus studies (Bonacum et al. 2011; Williams et al. 2012). We neglect nuclear genes (e.g., 28S or histone 3) because sequencing efforts have been limited in nautilus, precluding comparative analysis with past studies, and have been shown to be relatively uninformative for phylogenetic studies within this genus (Wray et al. 1995).
Now while the two species might indeed be one, you can’t conclude that from the identity of just two mitochondrial genes. And the Nautilus article at the top implies that a lot of DNA was examined. There may be substantial differences in other parts of the DNA that produce the morphological differences between the two (ergo these differences having a genetic rather than an epigenetic basis), and may even lead them to be reproductively isolated, ergo being two biological species.
I may have missed another paper looking at whole-genome sequences, but I doubt it. To me it seems that Ward is exaggerating his findings, and also implying that they extend to many species on earth, which might not be “biological” species because their differences are based not on DNA, but on developmental differences induced by the environment (and perhaps inherited via methylation). That might be true, but it’s an unwarranted extrapolation from a study of one organism.
Now Ward does mention one well known and important epigenetic property: the development of different cells and tissues in a single organism is often set off by epigenetic modifications that are themselves coded in the genome (i.e., the DNA of gene A says, “turn on/off genes B, C, D, and E under different internal environments”). Those differences are inherited through different cell divisions, which explains why, though all the cells in the body are genetically identical, they do different things and form different tissues. And those epigenetic changes are coded into the organisms’s DNA; they don’t come directly from the environment.
But that applies only to development of a single organism. It’s a very different thing to claim that environmental modification of the DNA of an organism is passed on through its gametes to its children, grandchildren, and so on, for that’s the only kind of environmental modification that can be involved in evolution. And the evidence says that this isn’t likely to happen. As I’ve said repeatedly, methylation changes (and Ward notes this) are usually wiped out completely when gametes are formed, and we know of NO adaptation that is caused by environmentally-induced methylation of DNA or histones.
Yet in his popular article, Ward goes on to imply that this really does happen, and happens in human evolution as well. Here are a few excerpts (my emphases):
The methyl molecules are not physically passed on to the next generation, but the propensity for them to attach in the same places in an entirely new life-form (a next-generation life-form) is. This methylation is caused by sudden traumas to the body, such as poisoning, fear, famine, and near-death experience. None of these events come from small methyl molecules, but they cause small methyl molecules already in the body to swarm onto the entire DNA in the body at specific and crucial sites. These acts can have an effect not only on a person’s DNA but on the DNA of their offspring. The dawning view is that we can pass on the physical and biological effects of our good or bad habits and even the mental states acquired during our lives.
This is a stark change from the theory of evolution through natural selection. Heritable epigenetics is not a slow, thousand-year process. These changes can happen in minutes. A random hit to the head by an enraged lover. A sick, sexually abusive parent. Breathing in toxic fumes. Coming to God in religious ecstasy. All can change us, and possibly change our children as a consequence.
There is not a lick of evidence for any of that!
And there’s this:
. . . It has long been “truth” that the epigenome (the complement of chemicals that modify the expression and function of the organism’s genes, such as the methyl molecules that can glom onto specific genes during the life of the organism due to some environmental change) of the parent is reprogrammed (all epigenetic traces removed) twice: once during the formation of the gamete itself (the unfertilized egg, or a sperm waiting around to fertilize an egg) and secondly at conception. Erase and erase again. But now experiments definitively show that some of the chemicals added during the life of an organism do leave information in such a way that the offspring has [sic] their genes quickly modified in the same way that the parents did. The same places on the long DNA molecules of the newly born (or even the “not-yet” born) get the same epigenetic add-ons that one or both of the parents had. This is not supposed to happen. The revolution is the realization that it does. It happened to the nautilus. And it happens to you and me.
That is a gross exaggeration, and greatly misleading. If you want to see a good consideration and critique of the purported evidence for transgenerational epigenetic inheritance in humans, read this 2018 Wiring the Brain website post (click on screenshot) by Kevin Mitchell (note: he considers the overblown “Dutch famine” data as well):
Mitchell’s conclusion:
In my opinion, there is no convincing evidence showing transgenerational epigenetic inheritance in humans. But – for all the sociological reasons listed above – I don’t expect we’ll stop hearing about it any time soon.
He’s right on both counts: the evidence is horribly weak, and yet we still keep hearing about “Lamarckian” epigenetic inheritance, this time from Ward. After all, the message “Darwin was right” doesn’t sell books, but, in book publishing, “Darwin was wrong” is the scientific equivalent of “man bites dog”
As it says at the bottom of Ward’s article, these passages are from Lamarck’s Revenge. That doesn’t bode well for the book.
UPDATE: If you want a pdf of my article, which seems to be behind a paywall, just inquire judiciously.
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The journal Molecular Ecology is producing a special issue on “Sex chromosomes and speciation”, which will contain about 17 papers. Some of these have already been published online, and though there’s not yet a central link, some of the papers are here.
Since my lab more or less kickstarted the area by reviving interest in Haldane’s Rule and its probable cause by sex-chromosome evolution (see the paper for an explanation), I was asked to write a personal and historical introduction to the field to open the issue. My short paper can be seen by clicking on the screenshot below, which will lead you to a pdf of the manuscript—very close to the version that will be published.
I tried to write this paper so it would be accessible to not only general biologists, but also laypeople who are scientifically interested and a bit informed about evolution. I don’t know if I’ve succeeded, but, like Maru, I do my best.
This may be the next-to-last scientific paper I’ll ever publish, although it’s a short review rather than a data paper. However, a few colleagues and I are writing what may be the last real paper I’ll publish, chock full of data and, if I do say so myself, a nice piece of work. I think it’s a good way to go out. It’s been in the works for about a decade, since it took a long time to do all the morphological analyses and DNA sequencing, but I’ll say more about that later.
At least a dozen readers have called my attention to a new paper in Nature Communications by Anna M. Kearns et al. (reference at bottom, pdf here), supposedly showing “reverse speciation” in ravens. The paper has received a lot of public attention because it claims to show that two distinct species of ravens have fused back into a single species. And that has excited people because a.) they don’t think this has happened before, and b.) it shows that speciation is not the simple bifurcating tree that Darwin portrayed. Rather, some of the branches can grow back together, fusing into a new single branch.
But, as the authors note, we’ve seen fusion of species before. Often this is connected with anthropogenic habitat change, such as change in climate, local ecology, or the introduction of predators (see a summary paper here). We may be seeing this now with the polar bear and brown bear (“grizzly”). Previously isolated by ecological preference and adaptation (a genetically based “reproductive isolating barrier”), their ecological separation may disappear with climate change. As the brown bear moves north with warmer climate, it will invade the territory of the polar bear, and the two species can hybridize and have done so repeatedly in the wild. If the hybrids are fertile (and I can’t find data on this), the two species may well fuse into one.
But there are other cases of species fusing when humans weren’t responsible. After all, ecological change, climate change, and introduction of predators can occur without the intervention of humans. The problem with finding hybrid species in nature is that one can’t easily detect that they resulted from hybridization if the parental species are both extinct. (The hybrid nature of species is usually detected by seeing that they’re a genetic mosaic of the parental species, and if the parents don’t exist that’s hard to detect.) But we have plenty of example of “hybrid species” that haven’t replaced the parental ones, including many allopolyploid plants as well as diploid hybrid species in butterflies and sunflowers. Further, species do exchange genes more frequently than we used to think, and that “horizontal gene transfer” can mess up phylogenies.
But none of this invalidates the generalization that species nearly always form from geographically isolated populations that genetically differentiate to the point where they can no longer exchange genes, when they’ve evolved barriers to gene exchange like hybrid sterility, ecological preference and adaptation, mate discrimination, and so on. Except in plants, hybrid speciation is the rare exception rather than the rule, and Darwin’s “bifurcating tree” of life, drawn in his notebooks, is still a good description of life:
Now, what did Kearns et al. find? They found that two old lineages of Common Ravens (Corvus corax), one widespread (“Holarctic”) and one from the West coast of North America (“Californian”), had diverged, probably after geographic isolation, about 1.5 million years ago, but then didn’t become two extant species because they began exchanging genes—repeatedly. (The geographic isolation may have resulted from the common ancestor being isolated in refugia during times of glaciation.) So now, in the Western US and Mexico, one finds a raven that looks just like other worldwide ravens, but carries an ancient lineage of genes that must have diverged from the ancestor of “Holarctic” ravens a long time ago. That’s detectable because you find, in that area, birds that carry two gene copies that diverged anciently—far more divergent that the normal variation within Holarctic ravens.
At present, the California and Holarctic forms are not different species because they hybridize readily in Western North America, and there are no two distinct “types”. You can see them in the map below: Holarctic is purple, California is orange, and the hybrids, carrying genes from both, are striped purple-and-orange (the orange type is not found by itself; its genes have simply merged with those of the Holarctic ravens).
The situation is complicated because there’s another species of raven that is “sympatric” (lives in the same area as) both the Holarctic and California ravens but remains distinct: the Chihuahuan Raven, inhabiting the black area below. It’s regarded as a different and full species (Corvus cryptoleucus) because there’s no evidence that it hybridizes with any other group; it appears to be fully reproductively isolated from other ravens.
The distribution of the two lineages (and two species: Common and Chihuahuan) from the paper:
(From paper): (From paper): Reticulate speciation history of North American ravens. a Geographic range of distinct mtDNA lineages within Common and Chihuahuan Ravens based on previous mtDNA studies and range records.
What the authors discovered from DNA sequencing was that in fact the Chihuahuan Raven is more closely related to the California lineage of the Common Raven than to the Holarctic Raven, and apparently split off from the California isolate more recently than the divergence of the Chihuahuan and Holarctic lineages of the single Common Raven. The Chihuahuan branch split off from from the California lineage between 0.6 and 1.5 million years ago.
So what we have is shown in the diagram below: a non-bifurcating family tree. It reflect the ancient divergence of the lineage that produced the Holarctic branch of the Common Raven on one side and the Chihuahuan Raven + California lineage on the other. That branch then split again and more recently, producing the full species the Chihuahuan Raven and then the lineage of Common Raven that fused back with the Holarctic lineage. This should be clear from the diagram:
(From paper): b Hypothesis of speciation reversal where the Common Raven is formed from the fusion of non-sister California (orange) and Holarctic (purple) lineages following secondary contact, while Chihuahuan Ravens (black) remained reproductively isolated despite sympatry with the Common Raven. Dashed lines in b show the mtDNA gene tree topology from this and previous studies. Solid grey background in b traces the changing taxonomic boundaries as the Holarctic lineage first split from the ancestor of the California and Chihuahuan lineages, and then the California and Holarctic lineages fused into a single admixed lineage
The upshot: The big question, and the reason this paper got so much publicity, is the claim, echoed in the paper’s title, that it showed “speciation reversal.” That is, the authors assume that the California lineage was once a species of raven distinct from the Holarctic Common Raven, but then fused with it later. Somehow the reproductive barriers (genetic ones) that kept them apart became ineffectual.
That, of course, assumes that there were once reproductive barriers between the California and Holarctic lineages. But we have no evidence for that! The fact that they fused so easily, and without human intervention, argues against substantial reproductive barriers, though there could have been some ecological ones. The authors simply assume that, because the Chihuahuan raven became a full species in less time than the Holarctic-California divergence, then the latter divergence must ALSO have involved full speciation.
But divergence time tells us very little about speciation. The key is whether a lineage evolves reproductive barriers from another one, not how long they’ve been separated. And those reproductive barriers are probably byproducts of selection, which can be either strong or weak. That’s why, when judging whether two populations are biological species, evolutionists prefer to use indices of reproductive isolation (observations of no matings, no evidence of genetic admixture) rather than divergence times. It may be, with the Holarctic and California lineages, that they simply didn’t diverge genetically enough to produce reproductive barriers as a byproduct. That’s what happened to Homo sapiens: our own geographic isolates in Polynesia, Australia, and the New World weren’t separated long enough from the rest of the species to become new species of humans. Now that we have transportation and migration, we’re in the process of slowly fusing into one big gene pool, which may never be fully mixed but mixed enough to keep us able to mate with people from every other place.
The authors recognize this problem but, perhaps recognizing the extra attention that “speciation reversal” will get (as opposed to “lineage reversal”), make the flawed “time argument” for speciation (my emphasis in the quote):
Thus, it is not clear-cut whether we should call the situation in ravens ‘speciation reversal’ or view it as a case of ‘ancient lineage fusion’. This contrasts with most other examples of speciation reversal, where there is strong evidence for the strength and nature of reproductive isolation prior to speciation reversal despite a very shallow divergence between lineages (e.g., sticklebacks). Two lines of evidence suggest that California and Holarctic lineages could have been reproductively isolated prior to secondary contact and lineage fusion. First, the timing of divergence of the Holarctic lineage and the ancestor of the California and Chihuahuan lineages between 0.9 and 2 mya (Supplementary Fig. 1) is approaching the limit where most bird taxa (especially those in the northern hemisphere) have evolved reproductive isolation (~2 mya). Second, life history traits, as well as mtDNA, intron, SNP and ENM analyses all support reproductive isolation between Chihuahuan Ravens and Common Ravens despite the more recent divergence of the Chihuahuan Raven and the California lineage 0.6–1.5 mya (Supplementary Fig. 1). This shows that ravens can develop reproductive isolation and maintain strong species boundaries after a more recent divergence than that between California and Holarctic lineages. We argue that our findings represent the strongest support possible for the conclusion of speciation reversal given the inability to measure ancient prefusion reproductive isolation.
I am not convinced by either line of evidence that the Holarctic and California lineages were separate species. Speciation times can vary among taxa, and if selection is weak, lineages may not progress to full species for a very long time. Using data from other birds doesn’t settle the issue in this particular case. The second line of evidence isn’t really independent: the authors simply say that because the Chihuahuan Raven speciated in less time than the divergence between Holarctic and California lineages, the latter two must also have been species. That’s not convincing either. “Time to speciation” varies widely, even within a group, depending on various factors that include the strength of selection, the degree of geographic isolation, and so on.
So what we see here is lineage fusion, not species fusion. Even the authors recognize the problem in the bolded bit above, but they try to obviate that. Pity that the science journalists who wrote about this didn’t know much about speciation.
h/t: Michael, Jószef, Tom
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Kearns, A. M., M. Restani, I. Szabo, A. Schrøder-Nielsen, J. A. Kim, H. M. Richardson, J. M. Marzluff, R. C. Fleischer, A. Johnsen, and K. E. Omland. 2018. Genomic evidence of speciation reversal in ravens. Nature Communications 9:906.
There must have been more than a dozen readers who sent me links to the article below by Carl Zimmer in the New York Times (thanks, all!). I skimmed it but was more interested in the published scientific papers about the marbled crayfish. This “species”, if you can call it that (see more below), is parthenogenetic—that is, it reproduces without having sex. That means that all individuals are females, and males, who normally contribute sperm in the ancestor, are absent. The population of the marbled crayfish doesn’t need males, and a whole lake can be populated from a single individual. I think Zimmer’s going a bit overboard in saying that the new mutant is “taking over Europe”, but otherwise it’s a reasonable article.
But let’s look at the original papers (links and free access below) to see what’s going on.
It’s pretty simple to summarize, though a bit complex genetically. In 1995 a “marbled crayfish” appeared in the German aquarium trade, apparently originating from a single mutant individual that was a member of the species Procambarus fallax, the “slough crayfish”. Here’s what the marbled crayfish looks like, having a mottled appearance similar to that of its immediate ancestor P. fallax:
It’s the only parthenogenetic species of decapod crustacean known (the group contains shrimp, crayfish, lobsters and crabs); and it reproduces by apomictic parthenogenesis—an egg is formed simply by normal cell division, or mitosis, and it’s fertile. No sperm required! This gives a single individual the capacity to invade a habitat and populate it, something that’s possible in sexually reproducing organisms only if the female is inseminated.
That parthenogenesis, combined with the marbled crayfish’s omnivorous diet, means that this thing is a threat, and it is spreading, especially, as the paper of Gutekunst et al. shows, in Madagascar. Now the parthenogenetic habit doesn’t necessarily mean the species (it’s really a clone, as we’ll see in a second) will replace other crayfish. It may be ecologically different from not only other crayfish species, but also from its ancestor P. fallax, in which case it could persist alongside them. According to population-genetic theory, “mutants” like this are expected to replace sexual forms in the same species, but only if their ecology is the same. But its ability to eat anything and to invade freshwater lakes with single individuals, makes it a worrisome threat.
How did this thing form? Its formation is in fact the key to its ability to reproduce asexually. It is a triploid: instead of having the normal complement of 184 chromosomes (two sets of 92) it has three sets: 276. (That’s a lot of chromosomes—humans have only 46.) What probably happened is that an ancestral P. fallax produced a diploid egg with 184 chromosomes instead of the normal 92-chromosome haploid egg. That egg then fused with the 92-chromosome sperm of another individual of the species, giving rise to a 276-chromosome triploid.
The triploid can’t make viable eggs by the normal process of meiosis, as that would involve three chromosomes of each type trying to pair and then separate, which would produce a mess. If an egg was even formed by that process, it wouldn’t have full sets of chromosomes, but might be missing some and have extras of others, which, when fertilized, would produce a zygote (incipient offspring) whose development would be screwed up. It could, however, reproduce through normal cell division (mitosis), as that doesn’t require chromosomes to pair. And that’s how this new clone reproduces: producing eggs by simple division of somatic cells.
Along with this there must be some feature of the marbled clone that allows this triploid cell to develop on its own, without the need for fertilization by a sperm. (These clones can mate with P. fallax males, but the transferred sperm doesn’t contribute anything to the offspring.) We don’t know whether the feature that allows this clone to reproduce without sex is a genetic mutation, or is simply a byproduct of a cell having three sets of chromosomes.
To look at the origins of this thing, Gutekunst et al. sequenced its genome: the first full-genome sequence of any decapod crustacean. And what they found was what you’d expect on the origin theory above: the individual had three sets of chromosomes, with two of them nearly identical and one more divergent, but still within the ambit of a P. fallax genome. That means that the species surely originated, as predicted, from an unreduced egg cell of a P. fallax female fertilized by the sperm of another P. fallax male. And comparing the DNA of the clone with those from other arthropods, the authors found this phylogeny, showing the species clustering closest to a crayfish relative, Parhyale hawaiensis, an amphipod crustacean.
(from paper): Phylogenetic clustering of 138 orthologues from recently published arthropod genomes. Shimodaira–Hasegawa-like branch support <1 is indicated by numbers.
So what we have here is a clone that reproduces without sex, similar to those viruses and bacteria that reproduce without true meiotic sex (these microbes do have a way of exchanging some genes, though).
But is it a new species? The paper of Frank Lyko (reference below) says it is, naming the triploid clone Procambarus virginalis. On what basis does he deem it a new species? Not morphology, for there are no traits that can absolutely distinguish the triploid clone from P. fallax. But one can tell the clone genetically apart from the ancestral species because it has a diagnostic mitochondrial DNA. Yet that’s only because the first mutant individual had a unique sequence of DNA in the mitochondria (which all of us do!) that has been passed on to its clonal ancestors. To me, that’s just an arbitrary trait that enables one to tell the clone and ancestor apart, but has no biological significance.
Finally, Lyko notes that the clonal “species” is reproductively isolated from P. fallax: they can’t exchange genes. Reproductive isolation of one group from another is, of course, the biological hallmark of a species, so this deserves closer consideration. But that alone doesn’t mean that P. virginialis adheres to the classical biological species definition for this reason: individuals within the clonal species are also reproductively isolated from each other! The Biological Species Concept (BSC) notes that a species is “a group of interbreeding individuals that is reproductively isolated from other such groups.” But individuals of P. virginialis aren’t interbreeding: they can’t mate with each other!
Thus, the isolates of the clonal species, left alone in different lakes, could diverge via evolution indefinitely, and one would never be able to test their reproductive compatibility through either observing them in aquaria or seeing what happens if they once again regain contact. In both cases no matings are possible, and thus “interbreeding” cannot be judged.
This means that, like bacteria or other asexual groups, we can’t use the BSC to see if this clone represents a new species. Species delineation in such groups becomes a more or less arbitrary exercise based on degrees of genetic or morphological difference, and there’s no way to tell whether each population of the clone, left in a different lake, will become a different species. Is a single nucleotide difference in the huge genome, diagnostic for a lake, sufficient to delineate a new species within P. virginialis? If not, how much difference is necessary? This is why the species concept is easier to apply in sexually reproducing organisms: if they meet in nature, they either interbreed or not (there may, of course be problematic cases of very limited interbreeding, but in many groups those aren’t a problem).
By deciding to call this a new species, Lyko is making a judgment call—one very different from deciding that Drosophila simulans is a species different from D. melanogaster, since they co-occur in nature but never exchange genes (hybrids are sterile and most are inviable).
Other species of parthenogenetic animals have also been named, like the famous fish Poeciliopsis monacha-occidentalis, which arose by hybridization between two different species but has been asexual for over 100,000 generations. This, too, is now a clone, and the species designation is more or less arbitrary when one takes into account that there is nothing promoting interbreeding or preventing genetic divergence between groups of clones.
So that’s my take on whether this thing is a new species: it’s problematic because the crayfish is an asexual clone. The biology, however, is fascinating, and it would be nice to find out what feature of the single original triploid individual enabled it to reproduce without sex.
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 finchG. 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
A few days ago I was interviewed by Eva Botkin-Kowacki, a science writer for the Christian Science Monitor. She wanted to discuss a new paper on speciation in birds, a commentary published in The Auk by Geoffrey E. Hill of Auburn University: “The mitonuclear compatibility species concept” (free download, reference at bottom). She also interviewed several other evolutionary biologists and ornithologists.
Hill’s idea is that speciation in birds proceeds largely through the mitochondria of one isolated population evolving divergently from the nuclear genomes of another population, so when the populations encounter each other after a long period of isolation, the mitochondrial genes of one species are mismatched with some nuclear genes from the other, and the hybrids become either sterile or inviable. That would make them different species if the hybrid problems are severe as gene flow between the populations would be very low. The strongest evidence Hill has for his hypothesis is that for the two bird “species,” the blue-winged warbler and golden-winged warbler have very low divergence in the nuclear genes (0.03% to be exact), but the mitochondria differ much more strongly—3%. They are considered species because they have different markings and maintain their marking distinctness when they meet.
Hill’s “mitonuclear compatibility species concept” proposes that when a certain degree of genetic difference between mitochondria of different groups is seen, that is indicative of mitonuclear incompatibility, and the groups should be called different species:
As a result, once populations diverge in coadapted mitonuclear genotypes, the reduced fitness of offspring due to mitonuclear incompatibilities prohibits exchange of mt and N-mt genes and effectively isolates individuals with shared coadapted N and mt genotypes. Given these considerations, I propose that avian species can be objectively diagnosed by uniquely coadapted mt and N genotypes that are incompatible with the coadapted mt and N genotype of any other population. According to this mitonuclear compatibility species concept, mitochondrial genotype is the best current method for diagnosing species.
But he doesn’t say how much difference between mitochondrial DNA would mandate a diagnosis that two populations are different species.
To Hill, the warbler mtDNA divergence suggested that the big divergence of mitochondria played the major role in preventing gene flow between these species. But this is problematic for several reasons.
First, for a deleterious mitochondrial mt/nuclear DNA interaction, the nuclear DNA would have to have diverged as well in some places. We know that there are six regions in these species that have marked divergence in nuclear DNA, and these include the genes for body color (there are also ecological differences). But why couldn’t the speciation of these groups have involved sexual selection, so that they’ve diverged in both male color and female preference, rather than hybrid inviability due to mt/nuclear DNA divergence?
Or maybe ecological differentiation plays a role. One problem with Hill’s theory, pointed out by evolutionists Darren Irwin and Brian Sidlauskas in the Monitor piece, is that it assumes that nuclear/mtDNA incompatibility is the cause of speciation, when it could (if it even exists; see below) might have followed speciation that had already occurred through sexual selection or other processes.
But if that’s the case, why are the mitochondria so diverged compared to the nuclear DNA? I have my own theory on that, which I imparted to Ms. Botkin-Kowacki, but which she didn’t mention in her piece. In birds, females are the heterogametic sex (the sex with unlike sex chromosomes), having ZW females and ZZ males. This is the reverse of the situation in mammals and insects, in which males are heterogametic, with XX chromosomes in females and XY chromosomes in males (Lepidoptera are like birds in this respect.)
We also know, in a phenomenon called “Haldane’s Rule” (after biologist J.B.S. Haldane), that in hybrids between species and populations, if only one of the two sexes is sterile or inviable, it is almost invariably the heterogametic sex. So in species hybrids in birds and butterflies, the females are often sterile or inviable, while in mammals and insects it’s usually the males. I spent much of my career working on this phenomenon, and my work and that of others have suggested some explanations, which I won’t go into here.
If Haldane’s rule applies in these warblers, then the female hybrids could be more sterile or inviable than males. Since females but not males pass on mitochondrial DNA, this would—because female hybrids couldn’t mate with males of either parental species—prevent the mitochondrial DNA from moving between the two species. This wouldn’t apply to nuclear DNA, which could move between species when male hybrids mated with either parental species. But those male hybrids wouldn’t pass on their mitochondrial DNA, which is transmitted only by the female parent. This phenomenon alone would account for the disparity in mitochondrial versus nuclear DNA divergence, without having to invoke any bad interactions between mitochondrial and nuclear genes. It’s simply a phenomenon of genetics–if part of the DNA can’t move between species, then that part will diverge faster. And that would knock down Hill’s strongest evidence. (His evidence for his theory isn’t very strong anyway, though we have seen the phenomenon in some copepods).
There are other problems with Hill’s theory:
It’s subjective: how much divergence between mitochondrial DNA of two groups would make them count as different species? While the Biological Species Concept (BSC), which counts species as different if gene flow between them is severely impeded, is subjective in some cases of incomplete gene flow, in many others it’s objective: humans can’t exchange genes with chimps, or Drosophila simulans with D. melanogaster (hybrids are completely sterile or inviable).
Hill’s species concept is merely a subset of the BSC: it’s just one of many ways that gene flow can be interrupted, and we now of many species, like ducks, that maintain distinctness through other reproductive barriers not involving mt/nuclear DNA problems.
Hill’s species concept isn’t general: we know of many species in other groups for which gene flow is prevented not by hybrid sterility or inviability, but things like differences in ecology, mating preference, or time of mating, or use of different pollinators.
As Hill admits, there is no direct evidence in any bird species for hybrid problems being caused by deleterious interactions between the mitochondrial DNA of one species and the nuclear DNA of another. It’s a a purely speculative theory based on observations, like the warbler data, that have other and better explanations.
In other groups like mammals and flies, it is the mitochondria that move easily between species while the nuclear DNA is more divergent. This is explained by Haldane’s Rule (in those groups fertile hybrid females can move mtDNA between species), but not by Hill’s idea that mitochondria are genetically incompatible with nuclear DNA.
As I told Ms. Botkin-Kowacki, I thought Hill’s theory was somewhat interesting, but was surprised that she was writing an article on it since it wasn’t that earth-shaking. She replied that the idea of “species” is always being revised, and now there was yet another species concept. I then told her why I thought the BSC was the most useful one in understanding the “species problem” that intrigued evolutionary biologists during the Modern Synthesis, and my explanation is below:
Jerry Coyne, a biologist at the University of Chicago and co-author of the book “Speciation,” agrees that Hill’s hypothesis could only be one aspect of what is going on as part of the classic biological species concept. “He hasn’t established that this is a better criterion for a species concept than the one that is traditionally used,” Dr. Coyne says in a phone interview with the Monitor. “It always comes down to reproductive isolation.”
“If you ask why nature is lumpy,” he says referring to the groupings that scientists call species, “you can hardly arrive at any other conclusion other than that the things that would make these lumps a continuum instead of a lumpiness are reproductive barriers.”
Trying to find a one-size-fits-all species concept might not be the best approach for biologists, Irwin says. “It may be that different concepts work better in different groups of animals or plants and it may be that different processes are sort of occurring in different cases,” he says. “There may not be a perfect species concept.”
I don’t think there’s one species concept that covers both asexual and sexual groups (you can’t have reproductive isolation in a group that doesn’t reproduce!), but that the BSC has proven the most useful one in understanding nature’s discontinuity. I also told her that every paper of which I’m aware that discusses the process of speciation uses the BSC, so biologists implicitly realize that reproductive isolation is crucial in maintaining the distinct groups in nature we call species.
