I recently went to see the Cassia Crossbill (Loxia sinesciuris) in Idaho to add that species to my life list of North American birds. I wrote an earlier blog about this birding trip in which I stated that I was going to see this bird even though, as a scientist who studies speciation, I did not think that it should be recognized as a species. I want to explain why I hold that opinion about the Cassia Crossbill.
The Cassia Crossbill has the smallest range of any recognized species in North America that is not an island endemic.
I think it is important at the outset of this essay to be clear that I am in no way disparaging the fantastic research that has been conducted on crossbill evolution by my colleague Dr. Craig Benkman, who is a professor at the University of Wyoming. Dr. Benkman’s studies on the co-evolution of crossbills with Lodgepole Pine, their primary food source, and Red Squirrels, their primary competitors for pine cones, is among the best studies of avian evolution and the co-evolution of organisms ever conducted. The body of research published by Dr. Benkman and his students is on par with (and in many way surpasses) the classic studies of bill size evolution in Darwin’s Finches conducted by Dr. Peter Grant and is frequently and appropriately highlighted in textbooks alongside Grant’s Galapagos Finch studies. I have nothing but accolades for the studies of adaptive evolution of crossbills. I also have deep appreciation for the decades of careful field work that generated the observations that are the basis for this essay on speciation. I hold a different view of how to define a species than Dr. Benkman (and nearly every other evolutionary biologist), and therefore I disagree with his recommendation that the South Hills population of crossbills be elevated to species status. But this is a discussion of evolutionary concepts, not a personal criticism of Dr. Benkman or any other scientist.
Ultimately, although Dr. Benkman’s opinions carried a lot of weight concerning the species status of the Cassia Crossbill (which I will also refer to as the South Hills crossbill or the call type 9 population of crossbills) and the data generated by his lab group was the basis for discussions of the species status of the South Hills crossbill, decisions of whether or not bird populations in North America (which includes the entire continent to the southern edge of Panama) are distinct species or not falls to the North American Classification and Nomenclature Committee of the American Ornithological Society (hereafter the checklist committee). This checklist committee is composed of a dozen ornithologists, primarily professional university or museum faculty. (Ten committee members voted on the status of the Cassia Crossbill.) These members do not get paid—they conduct volunteer committee work as a service for the American Ornithological Society. According to the rules of the committee, a population of birds in North or Middle America is elevated to species status when 2/3 of the committee vote in support of species status. Species status can also be revoked by 2/3 majority vote. If you ever wondered about the mechanism by which species are added or subtracted from your field guide, it is the number of hands that are raised in a committee meeting. A terse summary of the rationale behind a committee decision is released when the checklist is revised, and voting committee members can (but are not required to) explain their votes in the committee report. The petition to elevate Cassia Crossbill to species status was voted down in first consideration in 2009 but was approved by an 8 to 2 vote in 2017. The rationale for votes was much clearer in 2009 than in 2017. You can view all of the published explanations for votes by searching around here.
A decision of whether or not to recognize a population of birds as a distinct species is based a species concept—a stated definition of species (You can read more about species concepts in an earlier blog that I wrote or in a mountain of other material available on the web). The officially accepted species concept that is to be followed by the AOS checklist committee, according to their stated philosophy, is a 80-year-old idea developed by the Harvard ornithologist Dr. Ernst Mayr known as the biological species concept. This species concept defines species by lack of exchange of genes with any other population; lack of gene flow is often called reproductive isolation but that term can be confusing because it does not necessarily have anything to do with mate choice or pairing. Accordingly, a population of birds is viewed as different from all other populations of birds at a species level only if it is reproductively isolated from all other populations. By this definition, even if hybridization events occur, they should not result in the flow of genes from one species to another. Hybrids should be genetic dead-ends thus isolating the gene pools of the parent species. When populations of birds are geographically separated such that there is no opportunity for hybridization—for example Red-shouldered Hawks in California that are geographically separated from eastern Red-shouldered Hawks by 1000 miles—members of the committee are left to speculate about whether individuals from the two population would hybridize and exchange genes if the opportunity arose. The biological species concept was developed before DNA was discovered and before scientists knew that mitochondria carried genes, but it has been adapted to some degree to a genomic age by holding to the idea that gene pool of species should be isolated from the gene pools of all other species.
Ernst Mayr was a prolific author and wrote multiple books and numerous articles in biology journals laying out the biological species concept in great detail. (I’ll add a short bibliography of key Mayr books and papers to the end of this blog.) The foundation of his biological species concept is the need for populations to exist in allopatry (physically separated with no opportunity for gene flow) for long periods of time as reproductive isolation evolves. In proposing long periods of separation, Mayr was invoking an evolutionary time scale—not a human lifespan time scale—not decades; not centuries; not even tens of millennia. At a minimum for birds, most ornithologists including Mayr invoke hundreds of thousands of years for reproductive isolation to evolve. The reason that so much time is required is that the diverging populations (incipient species if you will) need time to evolve fixed genetic differences in unique networks of genes that cofunction to achieve core organism function. Open any textbook on cell biology and look at the complex pathways that underlie core processes like water balance, endothermy, blood pressure, or immune defense. Those pathways are coded for by multiple genes and the products of all the genes in a pathway must co-function well or the key pathway will be compromised. Mayr referred to these as “adaptive gene complexes”. Mayr did not originate the idea of adaptive gene complexes but he saw adaptive gene complexes as key to creating barriers to gene flow between populations of birds. If populations come back into contact after they have diverged for long periods of time (this is often called secondary contact), then mixing genes from the adaptive gene complexes from one species with those of the other species could lead to the mixing of components in pathways that do not function well together, producing hybrid offspring with poor system function. This would render hybrids genetic dead ends and halt the flow of genes. To Mayr, reaching a point of hybrid incompatibility is the point at which the process of speciation is complete. Alternatively, the rapid evolution of morphological differences (like a different bill size) and very strong female mating preferences for the morphology of her population could theoretically stop gene flow and establish a new species. But, if mating patterns are all that stop the flow of genes, then even a few mistakes—one in a hundred pairings or even one in a thousand pairings—would lead to the flow of genes from one population to another and tear down species barriers. Mayr and other proponents of the biological species concept generally viewed mating patterns as a means to reinforce species boundaries (avoid mistakes leading to dysfunctional offspring), but they always come back to low performance of hybrids (post-zygotic—after mating—isolating mechanisms) as the key to the disruption of gene flow and the evolution of species boundaries. A core premise of the biological species concept is that hybrid dysfunction arises from the evolution of uniquely coadapted gene complexes that evolve in allopatry.
So, the core process of speciation according to the biological species concept as presented by Mayr is the physical separation of bird populations for long periods of time leading to the evolution of differences between the species that halt the flow of genes. The biological species concept is the stated species concept of the AOS checklist committee and it was this definition that was supposedly followed in elevating Cassia Crossbills to species status.
Now let’s consider the population of crossbills that breed in SE Idaho. To begin with, this is not an ancient lineage. It can’t be. The last glacial maximum in North America was only about 22,000 years ago, and so only a couple of tens of thousands of years ago a great sheet of ice hundreds of feet thick covered the area where Cassia Crossbills now live. The molecular data also points back to a common ancestor for all “Red Crossbills” to about 11,000 years before present (Björklund et al. 2013). The Red Crossbill complex would include Scottish Crossbills and Parrot Crossbills in Europe as well Cassia Crossbills in western North America and a generic “Red Crossbill” that is distributed (going east around the Earth) from England to Labrador. 11,000 years is a blink of an eye in evolutionary time, but Cassia Crossbills aren’t even that old. Based on climate models and projections of how long a red-squirrel-free South Hills lodgepole pine ecosystem likely existed in SE Idaho, Parchman et al (et al. 2016) concluded that “coevolution and genome divergence [of Cassia Crossbills] occurred within the last 6000 years”. Almost no other bird species (or vertebrate species for that matter) are proposed to have diverged within a period as short as 6,000 years (although for a radically different view that proposes avian speciation within decades see Hendry et al. (2007)). One hundred thousand years is usually considered the shortest time span for speciation in birds (Price 2015). Thus, the very brief existence of the population of Red Crossbills in the South Hills of Idaho necessitates that the claim of speciation be founded on a pace of speciation essentially unprecedented in North American ornithology. Because speciation in 6000 years seems so unlikely, one might assume that the data in support of species status is a grand slam. I agree with the phrase popularized by astrophysicist Carl Sagan: “Extraordinary claims require extraordinary evidence”. Avian speciation in 6000 years is an extraordinary claim.
First, let’s go old school and consider the species status of the population of South Hills crossbills as might have been done in 1942, when Mayr was crafting the biological species concept. Based on the behavior of the birds, is there reproductive isolation? The answer is yes (mostly). Benkman and his colleagues assessed 1704 crossbill pairs and found 12 pairs that involved one bird giving the Cassia Crossbill specific call type 9 along with a second crossbill giving another call type (Benkman et al. 2009). So, if we want to advocate for the uniqueness of the population, then we could state that there is almost no hybridization: less than 1%. However, if we want to hold to the Biological Species Concept, we cannot not ignore that there is regular hybridization between the putative endemic crossbill species and other crossbill populations. There certainly appear to be no strong barriers to mating between populations because Benkman et al. (2009) commented on how few opportunities there are for between-call-type pairings—the timing of breeding of Cassia Crossbills and other crossbills is typically out of sync (Benkman et al. 2009). This means that most of the call type 5 and call type 2 crossbills that live in the South Hills when Cassia Crossbills are breeding are not potential mates because they are not in breeding condition. Thus, with low opportunities for hybridization, we still see hybridization. This does not argue for a level of reproductive isolation that would stop the flow of genes between South Hills birds and birds from other populations. The same conclusion was echoed in mate choice trials in Benkman’s lab; 17% of female Cassia Crossbills showed a preference for males from other call types (Snowberg and Benkman 2007). And the hybrid pairings of South Hill’s type crossbills and other crossbills almost certainly result in fully functional offspring that go on to breed, dragging genes across species boundaries. How do I know that hybrids go on to breed? (Benkman never commented on it.) The lack of genetic structure of crossbill populations tell me that that they do—I’ll get to genetics in a second.
Perhaps the most startling aspect of the behavioral observations is that a bird was observed to switch call types! (Benkman et al. 2009). A bird of call type 2 copied the Cassia Crossbill call type of its mate! Essentially a call type 2 bird “switched teams”—it transitioned into a Cassia Crossbill just by changing its behavior. My jaw almost hit my desk when I read that. Call type is the diagnostic feature of these crossbills. Cassia Crossbills have a distinctive bill shape relative to other crossbills but it is not diagnostic because there is overlap in bill dimensions with other populations. The call type is discretely different and it is the diagnostic feature of this species, just as plumage pattern defines many species of birds. Imagine if one described a new species of bird based on a discrete plumage pattern that defines the new species (say a red cap and throat versus a blue cap and throat of a sister population), but then with banding data it was noted that some red-capped birds simply transitioned into blue-capped birds. There would be nothing left by which to diagnose the new species. Benkman and colleagues dismissed the switch of call types as insignificant with regards to species boundaries because it occurred after pairing, but the potential for call type switches seems very significant to me. Importantly, once we know that individuals change call type to match the call type of their mate, the count of only 12 pairs mismatched by call type becomes much weaker evidence for the reproductive isolation of these birds. I would have to be convinced that the 1700 pairs of birds with the same call types don’t include multiple hybrid pairs that have already synced their call types.
What about genetic divergence? In the 21st century, genetic divergence is a very important consideration in deciding the species status of a bird population. Analysis of DNA provides critical information about the extent of gene flow between two populations of birds—and remember, lack of gene flow is the basis for the biological species concept. Given that there would be every reason to doubt that a 6,000-year-old population of red crossbills that lives in sympatry with and mates with other populations of red crossbills could have reached species status, one would assume that the genetic data must absolutely nail the uniqueness of this population. To the contrary, however, the genetic data supporting a species status for the Cassia Crossbill are not convincing. Initial studies based on both mitochondrial and nuclear gene sequences failed to find any fixed differences between the South Hills crossbills and any other population of crossbills (Questiau et al. 1999, Parchman et al. 2006). After assessing divergence in both nuclear and mitochondrial genes in crossbills from throughout Eurasia and N American and including the South Hills population, Questiau et al. (1999) concluded in a paper in the journal Heredity “Morphological differentiation . . . shows the possibility of rapid local adaptation to fluctuating resources … without necessarily promoting the development of reproductive barriers between morphs.” In other words, there is local adaptation but no hint of species-level divergence in genotype. In the first genetic analysis from Benkan’s group, which was based on nuclear DNA markers, Parkman, Benkman, and Britch (2006) concluded that their analysis “did not separate individuals from the eight call types in the red crossbill complex, consistent with recent divergence and ongoing gene flow.” So again, no biological species here—and actually—in both the Questiau and Parkman et al papers, the genetic data indicated substantial on-going gene flow with other crossbill populations (hence the reason that I know that some hybrid offspring go on to reproduce, dragging genes across population boundaries). Remember the definition of a species according to the biological species concept: a population that is isolated from gene flow with any other population.
The genetic analyses of crossbills up to the 2006 paper by Parkman, Benkman, and Britch were limited by the available technology to analyzing a small sample of the genomes of the crossbills. By a decade into the twenty-first century, however, the sequencing of DNA was getting cheap enough that a lot more of the nuclear genomes of crossbills could be compared. And comparisons could be made not just of fragments of DNA but individual nucleotides (remember each nucleotide is a letter in the genetic code: A or T or G or C). In 2016, Benkman’s group compared almost 240,000 nucleotide positions (called SNPs in technical journals) in the DNA isolated from 230 individual crossbills drawn from all North American call types, including, of course, the South Hills (call type 9) birds. When the researchers then used a clustering algorithm to see how the pattern of shared and different nucleotides grouped the crossbills, they found that in the 90% of clustering runs, the South Hills Crossbills clustered as one group. 10% of the time, the clustering of DNA similarities/differences did not cleanly separate South Hills crossbills from other crossbill populations. It was this comparison of SNP data above all else that convinced the checklist committee to elevate Cassia Crossbills to the status of unique species. But in the age of 23andMe and Ancestry.com, the average person can now appreciate that widespread species (like Red Crossbills or Homo sapiens) will show a lot of genetic structures with differentiation among local populations that are certainly not species. Based on a SNP analysis similar to what was used in the crossbill study, 23andMe was able to assign me to a western European population of Homo sapiens with better than 95% confidence (and the written and oral history of my family supports the accuracy of this assignment). The bottom line here is that people can be assigned to human populations via SNP analysis more definitely than crossbills collected in the South Hills can be assigned to Cassia Crossbill. It is worth noting that there are many other populations of birds that are more diagnosable than Cassia Crossbills with much deeper genetic divergence that do not hold species status. I am certain that human populations are not different species. I’m also confident that many populations of birds that can be sorted only by analysis of hundreds of thousands of SNPs are not species. And I’m adamant that the crossbills in the South Hills of Idaho should not be recognized as a species.
When Benkman and his colleagues proposed that this was a new species of bird, they invoked the biological species concept as their criteria assessing the species status of crossbills. Likewise, the stated species concept for the checklist committee is the biological species concept. Based on the arguments that I present in this essay, the Cassia Crossbill fails to meet the criteria of this species concept. In the introduction to their paper, Benkman et al. (2009) vacillate a bit in invoking the Biological Species Concept by saying they follow a Biological Species Concept with gene flow. That is an oxymoron. A biologist stating that he or she embraces the biological species concept but allow for gene flow between taxa is like an economist saying they embrace laissez-faire economics, but encourage that prices of key goods be fixed by a government. When prices are fixed, you no longer have laissez-faire economics and when significant gene flow occurs among populations, you no longer have biological species. I personally hold to the idea that you can have a lot of gene flow between species—just not mitochondrial genes or the nuclear genes that cofunction with them (see my blog post which I reference above). But the mitonuclear compatibility species concept does not save the Cassia Crossbill and doesn’t need to be discussed further here.
Why does it matter whether we call the population of crossbills in the South Hills a species, a subspecies, a population, or an ecomorph? As an evolutionary biologist interested in the process of speciation, I think it matters a lot. I see a growing confusion among evolutionary biologists about the process of species (see a critique written by Robert Zink and me about the incredible claim that speciation can occur within 3 generations (Hill and Zink 2018)). The elevation of Cassia Crossbill to full species is a manifestation of that confusion. There is currently great enthusiasm for the idea that speciation can occur within a population of birds without geographic isolation if two subpopulations are subject to disruptive selection (like sedentary/lodgepole specialists versus nomadic cone generalists in the case of crossbills). Assumption-laden mathematical models can get this to work (maybe), but examples in nature do not hold up under scrutiny. The Cassia Crossbill is now commonly cited as vindication for the idea. With precedence established, we can expect the splitting of other populations of birds that are not genetically distinct thereby establishing more (false) precedence for this idea that birds commonly speciate in sympatry.
The erroneous (in my opinion) interpretation of local adaptation by Red Crossbills in the South Hills was foreshadowed by a remarkably similar mis-interpretation of response to natural selection in Darwin’s Finches on the Galapagos Islands (see Hill and Zink (2018) for a recent discussion). Fantastic long-term studies of both South Hills Crossbills and populations of Darwin’s Finches in the genus Geospiza established how populations could respond to directional natural selection—in both cases on the size and shape of beaks—and rise toward local peaks of adaptation. Ernst Mayr had also recognized this phenomena decades earlier and drew a sharp distinction between what he called “ecotypic variation” and “typostrophic variation”(Mayr 1954). Ecotypic variation, which is what is observed in Darwin’s Finches and Red Crossbills, is divergence of a local population that is still connected to a parent population via gene flow. Mayr was adamant that there is no expectation that ecotypic variation would lead to speciation unless gene flow was stopped by allopatry. Typostrophic variation, in contrast, is the differentiation of populations in allopatry. The non-overlapping divergence in morphology, behavior, and genotype between White-winged Crossbills and Red Crossbills is a clear example of typostrophic variation.
According to Mayr, it is key to grasp that the ecotypic variation is not incipient speciation. Dr. Robert Zink and Dr. Bailey McKay made this point brilliantly in an essay entitled “Sisyphean evolution in Darwin's finches” published in Biological Reviews (Mckay and Zink 2015). As many educated readers will know better than me, in Greek mythology Sisyphus was the king of Corinth and because of various misdeeds, we was condemned by Zeus to forever push a boulder toward the top of a hill. But the boulder would never stay put, rolling back to the bottom each time it neared the crest resulting in an endless cycle (and torturous punishment for Sispyphus). McKay and Zink used the futility of Sisypus’ efforts with the boulder as an analogy for the potentially perpetual evolution toward adaptive peaks by local populations with no chance of ever reaching a stable point on such peaks. (I cut and pasted Fig. 3 from McKay and Zink's paper above). They wrote: “Instead of revealing details of the origin of species, the mechanisms underlying the transient occurrence of ecomorphs provide one of the best illustrations of the antagonistic effects of natural selection and introgression.” Thus it is, in my opinion, with the Cassia Crossbill population in SE Idaho.
Benkman, C. W., J. W. Smith, P. C. Keenan, T. L. Parchman, and L. Santisteban (2009). A New Species Of The Red Crossbill (Fringillidae: Loxia ) From Idaho . The Condor 111:169–176. doi: 10.1525/cond.2009.080042
Björklund, M., D. Alonso, and P. Edelaar (2013). The genetic structure of crossbills suggests rapid diversification with little niche conservatism. Biological Journal of the Linnean Society 109:908–922.
Hendry, A. P., P. Nosil, and L. H. Rieseberg (2007). The speed of ecological speciation. Functional ecology 21:455.
Hill, G. E., and R. M. Zink (2018). Hybrid speciation in birds, with special reference to Darwin’s finches. Journal of Avian Biology 49:e01879.
Mayr, E. (1954). Change of genetic environment and evolution. In Evolution as a Process (J. Huxley, A. C. Hardy and E. B. Ford, Editors). Allen & Unwin, London.
Mckay, B. D., and R. M. Zink (2015). Sisyphean evolution in Darwin’s finches. Biological Reviews 90:689–698. doi: 10.1111/brv.12127
Parchman, T. L., C. W. Benkman, and S. C. Britch (2006). Patterns of genetic variation in the adaptive radiation of New World crossbills (Aves: Loxia). Molecular Ecology 15:1873–1887. doi: 10.1111/j.1365-294X.2006.02895.x
Parchman, T. L., C. A. Buerkle, V. Soria-Carrasco, and C. W. Benkman (2016). Genome divergence and diversification within a geographic mosaic of coevolution. Molecular Ecology 25:5705–5718. doi: 10.1111/mec.13825
Price, T. (2015). Speciation in Birds. In. W. H. Freeman, New Yok, New York.
Questiau, S., L. Gielly, M. Clouet, and P. Taberlet (1999). Phylogeographical evidence of gene flow among common crossbill (Loxia curvirostra, Aves, Fringillidae) populations at the continental level. Heredity 83:196–205.
Snowberg, L. K., and C. W. Benkman (2007). The role of marker traits in the assortative mating within red crossbills, Loxia curvirostra complex. Journal of Evolutionary Biology 20:1924–1932. doi: 10.1111/j.1420-9101.2007.01372.x
Some key works by Ernst Mayr that consider the process of speciation:
Mayr, Ernst (1942). Systematics and the Origin of Species. New York: Columbia University Press.
Mayr, Ernst (1963). Animal Species and Evolution. Cambridge: Belknap Press of Harvard University Press.
Mayr, Ernst (1970). Populations, Species, and Evolution. Cambridge: Belknap Press of Harvard University Press. I
Mayr, Ernst (1976). Evolution and the Diversity of Life. Cambridge: Belknap Press of Harvard University Press.
Mayr, Ernst (1982). The Growth of Biological Thought. Cambridge (Mass.): Belknap P. of Harvard