Why does the lay public tend to view hybridization in wild nature as a bastardization of the way things ought to be? Why do we favor “pure” species while rejecting hybrid crosses, or treating them like side-show freaks á la pizzlies, ligers and tiglons? I’ve been thinking a lot about hybridization lately, trying to wrap my head around not only how society views hybrids, but what role hybridization plays in diversity and fluffing the leaves and branches of the Tree of Life. And so it was with great interest that I read James Mallet’s review article in Trends in Ecology and Evolution titled “Hybridization as an invasion of the genome.” {1} It was published in 2005 within a special issue focused on biological invasions. Mallet looks at both the frequency of natural hybridization across taxa and also discusses how hybridization and introgression events may play a role in speciation, adaptive radiation and diversity. Hybridization, Mallett argues, is actually a lot more common across both the plant and animal kingdoms than biologists had previously thought. {2}
In Mallet’s view, hybrids are not always unnatural aberrations that represent a “failure” of isolating mechanisms that reinforce a species’ boundaries. Rather, some hybrids form important bridges of gene flow between two species, he argues. Hybridization is only one step of the process though, when it comes to shuttling genes across taxa. For this to happen, the hybrid individual must be fertile and it must mate with an individual from one of its parent species populations — let’s call it species-B. Then, it’s offspring must also mate within species-B, thereby perpetuating genes from species-A into the species-B population. This process is called introgression, when alleles from one species find their way in to the genome of a different — but usually closely related — species.
Mallet notes that while hybrids are rare on a per-individual basis, they are relatively common on a per-species basis. In fact he calculates that while 25 percent of plants are known to hybridize (no surprises there), about 10 percent of animals are currently hybridizing. (He excludes from this analysis any species thought to be hybridizing mainly due to human-induced reasons, such as habitat degradation.) Mallet cautions that this estimate may be on the low side and is a bit misleading, because certain “phylogenetic hotspots” have very high hybridization rates that swell well past the 25 percent mark set by plants (which is kind of surprising). He calculates that 100 percent of British grouse species (all four species within the family Tetraonidae) are currently hybridizing with at least one other species; nearly three-quarters of British ducks (Anatinae) hybridize; and about 43 percent of birds of paradise (family Paradisaeidae) are mixing it up. Certain butterfly families are known to be prone to hybridize too, with nearly 35 percent of the species within the genus Heliconius hybridizing, and it turns out that about 47 percent of North American swallowtails are swingers too. He calculated that six percent of European mammals are hybridizing — and I wish that he’d broken out some examples of certain families or genera, but alas, he didn’t. {3} Despite these high per-species rates, he calculates that the hybridization rate per individual is less than .1 percent, in most cases.
One thing I really appreciated about this paper was Mallet’s thoughtful explanation of how the very definition by which evolutionary biologists qualify what a species is affects their perspective of what hybridization is. As I’ve written about before, biologists struggle to devise a definition of species that operates across all the taxonomic kingdoms. Mallet argues that when the Biological Species Concept was widely used and in vogue in the 1950s and 1960s, that it’s strong reliance upon reproductive barriers as an isolating mechanism set up hybrids to be an aberration from the get-go. Supporters of this species concept often explained hybridism as a breakdown or interruption in these natural barriers, which they they usually attributed to human intervention (such as habitat degradation or introducing non-native species). They viewed these interventions as a disturbance of the natural balance, a perversion of the natural order.
While Mallet doesn’t disagree that human-induced interventions can lead to hybridism, he also asserts that that’s not where the story of hybridism begins and ends. He posits that the strengths of isolating mechanisms vary widely across taxa and that though human intervention can accelerate hybridization rates, there must have been some a priori gene flow occurring between the hybridizing species. Which means that some degree of hybridization is natural in the animal kingdom, but that human intervention and disturbances can amplify or accelerate this background rate.
Mallet also argues that the occurence of hybrids has likely gone under-reported in the animal kingdom because morphometrics alone can obscure hybrid offspring, which may be unwittingly grouped with one parent species or another. Hybridization in birds and butterflies, on the other hand, especially those with colorful plumage or patterning, is more easily recognized visually and therefore more widely studied. But because molecular tools have become so refined in recent years, hybridization can be better detected by using genetic markers specific to a species. Which makes me wonder if perhaps the DNA barcoding projects will, one day in the future, assist at better identifying hybrids and accruing data to calculate even finer-resolution hybridization rates, especially among mammals.
He also states that it’s generally the geologically-young species that have recently diverged which are more likely to be hybridizing. This suggests that there may be an evolutionary role for gene flow exchange between recently diverging species, and that there may be some sort of rough clock-like manner in which there is a window of time after species have diverged that they remain open to introgression. Mallet wrote:
For instance, in Heliconius, abundantly hybridizing geographic races within species almost all have mtDNA sequence differences of less than 2%; species that hybridize occasionally in the wild are mostly 2–6% divergent; whereas no hybrids are found between species 10% divergent. These results suggest that reproductive isolation between pairs of overlapping species evolves gradually and progressively, albeit somewhat irregularly. (pg. 232)
But the passage of time since two species diverged from each other phylogenetically — while important — is not the only bounding factor affecting two species’ ability to hybridize. Mallet also discusses the proclivity of certain taxa to hybridize by comparing the rate of hybridization among mammals of Europe (6 percent) to birds of the world (9 percent). He argues that previously mammals were thought less prone on the whole to hybridize because the “faster rates of mammalian developmental change and regulatory gene evolution cause a more rapid accumulation of hybrid incompatibilities” (pg. 233); and yet, the hybridization rate of European mammals is not largely different than birds of the world, which were considered based on lab experiments to have a higher hybridization rate than many other animal groups.
This is where I’m reminded of an ichthyologist who once chided me that “gene trees are not the same as species trees.” This is a hugely important point, because the fact there is gene flow or that a gene flow event happened within a species history does not negate that species’ status as a taxonomic or evolutionary unit. Sure, such events make it harder to define unequivocally what a species is — and it causes headaches for conservationists trying to devise policy for small populations or imperiled species — but it does not disqualify the organism from making progress on its evolutionary arc. Overall, this was a very thoughtful and eye-opening paper for me to chew on, and it gave me ever more food for thought for trying to better understand the porous species boundaries in Canis.
NOTES:
{1} Mallet, J. (2005). Hybridization as an invasion of the genome Trends in Ecology & Evolution, 20 (5), 229-237 DOI: 10.1016/j.tree.2005.02.010
{2} As always, I remind readers that I am not a scientist. If you see something in here that I’ve misinterpreted, please kindly let me know so we can all be the wiser.
{3} Even though he didn’t list mammals, he cited these two works on hybridizing European mammals:
MacDonald, D. and Barrett, P. (1995) European Mammals. Evolution and Behaviour, Harper Collins
Arnason, U. et al. (1991) Molecular identification of hybrids between the two largest whale species, the blue whale (Balaenoptera musculus) and the fin whale (B. physalus). Hereditas 115, 183–189
24 thoughts on “Givin’ props to hybrids”
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Kevin Z
Great article! Gotta love them hybrids. I am starting a PhD program at UNCW in August and will be looking into the maintenance of a mussel hybrid zone in the Gulf of Maine.
DeLene
Thanks Kevin, for some reason I thought you’d just finished up a PhD with Duke? Is this a second one? I found his idea of closely-related and young sister taxa being more prone to hybridization really interesting. It just makes sense. As you know, this is related to my interest in eastern wolf x coyote hybrids (so-called coywolves) and red wolf x coyote hybrids. I think this would fit with the current interpretation that they diverged from a common ancestor fairly recently. Have the mussels you are studying recently diverged, and are they sympatric?
Kevin Z
I’m a research technician at Duke. I have a Masters from Penn State.
The mussels are sympatric and I will learn more about their evolutionary history when I start this fall!
Neil
Awesome post, I look forward to reading the paper.
I think that the observation that the incidence of hybridization declines with increasing time of divergence between taxa sort of reinforces the notion that mating barriers are important in promoting and maintaing species differences. What’s not yet clear is whether these barriers are more influenced by selection against hybrid (and hybridizing) individuals, or is more of a by-product of say ecological differentiation (fewer encounters via niche displacement, behavioral differences) or differences in developmental pathways etc. I suppose all of these are probably at work to some degree.
Still, I entirely accept the thesis that hybridization has been unfairly derided and dismissed (starting with Darwin in chapter 8 of the Origin) as an important biological phenomenon. There is mounting evidence that hybridization, especially in plants, can actually be a pathway to the evolution of new species which is pretty amazing.
Also, while it’s true that generally more recently diverged species are more apt to hybridize there are some amazing cases of intergeneric hybrids that span millions of years of divergence (among whales, skinks, baboons, ducks and many plant groups). And there are some surprising cases where apparently closely related species maintain their ability to hybridize with distant relatives but not with each other (ducks in the genus Aix for example).
And am I the only one that thinks that top photo is mighty suspicious? (or maybe that’s the point…?)
DeLene
Hello Neil, you raise some great points that I need to educate myself on further — can you suggest any papers or sources for me to look into (regarding the various mechanisms you outline in your second paragraph)? About the photo, I have no idea if its a fake or not, maybe I ought to change it. I’d thought that tiglons were crosses with female lions and male tigers, but that mane would mean a male lion — hmmm…
Neil
The literature on the mechanisms of reproductive isolation is vast (a google scholar search turns up over 1,000,000 papers!) The Grants recently published a book summarizing their decades of work on the Galapagos finch complex called How and Why Species Multiply (2007). It is a nicely written introduction to the subject, but I think they have a tendency to generalize their observations of one (admittedly well-studied) case to animals as a whole. Nevertheless it is an easy read that introduces the key concepts with concrete examples and provides a good jumping off point.
Another good place to start is a classic review by Palumbi:
S R Palumbi “Genetic Divergence, Reproductive Isolation, and Marine Speciation” Annual Review of Ecology and Systematics 1994 25, 547-572 doi:10.1146/annurev.es.25.110194.002555
It is focussed on marine species and might be a bit dated, but much of it has relevance for terrestrial groups as well and it is pretty widely cited.
Alan
Great post. Here in Bristol in the UK we have a major centre of diversity in various species of Sorbus (whitebeams and rowans). Since I doubt that Sorbus was present in the area during the last glaciation, this means that 10+ distinct taxa have been generated by hybridization events between the parent species and the hybrids since then just in a very small area – at least one in the last 100 years or so as a result of a cross between a native rowan and a himalayan species grown as an ornamental tree.
david winter
Very nice,
If you are interested in the “speciation clock” one of the classic papers (if 5 year old papers can be classic) is
Bonick and Near Tempo of hybrid inviability in centrarchid fishes (Teleostei: Centrarchidae). Evolution: 59:1754-1767
Which will set you up for Haldane’s rule and a couple of associated ideas, combine that with the other suggestions above and you’ll be about read to to write a PhD on your wolves ;)
DeLene
Thanks very much for the references David, I’ll add them to my “need to look into” list.
michael
Just a quick comment on hybrids and science. I’m a scientist myself, but I’m also a critic of science. Scientists recently “discovered” that mice have “facial expressions” and show fear, and that dogs do as well. Well, any second grader could have told you that dogs show facial expressions 500 years ago (if they had second grade back then). That dogs smile and even laugh. That they show wonder, fear, hesitation, worry, excitement, pain etc…
The problem with science and scientists, is in their rules, (or lack of imagination in their experiments, or the baggage from centuries ago scientists who said that animals were machines who do not feel pain) often get in the way of allowing scientists to see the blindingly obvious.
But that’s not important right now…Let’s talk hybrids. Love hybrids, and like to take advantage of a hybrid vigor when I end up with a cast off dog (which are the only kind I ever get). I never go out and buy a dog. I end up with other people’s cast offs, because they can’t handle them or train them. These are my favorite kind of dogs, because it usually means they are smart and energetic. And it often means they are cross breeds.
Here’s the other thing about science and “species.” As humans, and as scientists, we think it’s our job to have rigid categories. To taxonomize everything down to meticulous detail.
Life is not like that. “Species” are not necessarily like that. They are constantly changing, constantly evolving. A moving target. The definition of a “species” will never be completely accurate because life will not cooperate with our desire for perfection.
It is imperfection and irregularity which are the genius of nature and evolution and life itself.
DeLene
I really don’t follow your logic Michael, because regardless of whether you classify dogs as Canis lupus familiaris or Canis familiaris, they are still all one species, though with various breeds… so a mixed breed dog is not a hybrid species unless you are talking about wolf-dog hybrids, or coyote-dog hybrids?
michael
Sorry, hybrid vigor (heterosis) is a more of an term of intraspecific population genetics within a species (although with the gray areas, I’m sure it is used to describe things such as the interspecific coywolves situation you have highlighted).
Whereas populations of wild species (such as the wolf) can be separated by things such as mountain ranges, deserts, etc.. dog populations are separated by humans who insist on having pure breeds and keeping them separate. When the breeds cross (usually by accident), it’s the same thing as if, say a mexican wolf somehow itself mating with a gray wolf.
Hybrid vigor is hybrid vigor and it happens in agriculture (plant and animal), dogs, coywolves when individuals from previously separated populations are bred or breed.
michael
Just a little more, if you don’t mind, because this subject totally fascinates me.
I tend to think in terms of “populations” and less in terms of species and subspecies, since there is so much disagreement among experts, especially with all the dog and wolf/red/mexican etc.. situations that you have covered so well. Some experts like to lump the subspecies all together, others like to have the finite lines.
Me….not overly concerned about the classifications. I’m a big picture guy. Just looked up “population” on wikipedia and it had an interesting definition
“A population is a set of organisms in which any pair of members can breed together. This implies that all members belong to the same species and live near each other.[1]”
It “implies” they are members of the same species, but does it DEMAND that they all be members of the same species?
In a sense, all Canis species in North America are a meta population, in that they can all interbreed. So… if this was that Discovery show “the End of Humans” or whatever it was called (showing life as it would be if humans went were no longer here), all the Canis species really would be free to intermingle and there would be massive gene flow, probably for centuries, until (if ever) it all sorted itself out.
things that make you go hmmmmm????
I plan on being one of a small clan of humans who somehow survive the apocalypse, and I will come out of a cave, with my solar powered video camera and film what happens.
DeLene
I really would not follow Wikipedia for this kind of thing… the definition you cite relies upon the Biological Species Concept’s reproductive barriers … and I think this definition falls flat on its face when applied to Canis.
michael
Yes, of course, I’m kind of mixing the “biological” concept of population with the more colloquial concept of population (sorry if I tend to do these things, because, like I have admitted, I don’t always play by the rules of science). The rules sometimes get in the way of my free thinking.
So, basically, there are a huge population (not the biological kind) of canids in the US. They can all interbreed resulting in coydogs, dogotes, coywolves, wolfdogs, carolina dogs, regular old dogs, maybe even some dingoes floating around.
It’s a big mess for the reproductive barrier type folks. But I’m not one of those folks. Just someone who likes to zoom out and look at the big picture more than he likes to zoom in and look at the fine lines.
Serge Dumont
Personally, I also liked the following books on speciation and hybrids:
1) “Speciation in birds” by Trevor Price
2) “The Birds of Northern Melanesia, Speciation, Ecology and Biogeography” by Ernst Mayr and Jared Diamond
3) “The Speciation & Biogeography of Birds” by Ian Newton
Regarding hybrids, I am working on a bird hybrids database that you can consult freely at:
http://www.bird-hybrids.com
I expect much more data on “cryptic” hybrids once the nuclear DNA data becomes available on the genomic scale.
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