Redpolls: genetically similar, phenotypically different

Redpolls are a group of small birds in the finch family, members of the genus Acanthis.  They breed in the far north, but sometimes migrate as far south as the central US in winter, when food is scarce further north.  They rely on a small variety of seeds, and sometimes travel a remarkable thousands of miles to find them.

Range of the Common Redpoll; Source: Cornell Lab of Ornithology

All redpolls share characteristic red markings on their heads, but otherwise these birds vary enough that they've been thought to comprise as many as six separate species, based on plumage and morphology.  Most commonly, ornithologists have treated them as three species; the Common Redpoll, the Hoary (or Arctic), and the Lesser.  Now a new paper ("Differentially expressed genes match bill morphology and plumage despite largely undifferentiated genomes in a Holarctic songbird," Mason and Taylor) reports a DNA sequencing study that suggests that the redpolls are in fact a single species.

Common Redpoll; Wikipedia Commons

Arctic Redpoll; Wikipedia Commons; (13667519855)" by Ron Knight from Seaford, East Sussex, United Kingdom -  Licensed under CC BY 2.0 via Wikimedia Commons

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Lesser Redpoll by Lawrie Phipps derivative work: MPF (talk) - Carduelis_cabaret.jpg. Licensed under CC BY 2.0 via Wikimedia Commons

A figure from the Mason and Taylor paper makes the differences more apparent:

From Figure 1, Mason and Taylor, 2015

As Gustave Axelson recently wrote in his post about this study for the Cornell Lab of Ornithology All About Birds blog, seeing a Hoary redpoll can be one of those Moby Dick-like quests for a birder intent on adding it to his or her lifelist.  But Mason and Taylor report, after sampling 77 redpolls of very different phenotype, and sequencing 20,000 SNPs in the genome, and 215,000 in the transcriptome (that is, mRNA transcribed from different genes), with gene expression data and ecological niche modeling, they find very little variation between the different redpolls. In contrast, as Axelson points out, genetic comparisons between other similar species of birds, such as black-capped and Carolina chickadees, has found substantial variation all across the genome.

Mason and Taylor write, "we present evidence of (i) largely undifferentiated genomes among currently recognized species; (ii) substantial niche overlap across the North American Acanthis range; and (iii) a strong relationship between polygenic patterns of gene expression and continuous phenotypic variation within a sample of redpolls from North America."

As evolutionary biologists, Mason and Taylor are interested in the processes that lead to phenotypic diversity and speciation. "The Holarctic redpoll finches (Genus: Acanthis) provide an intriguing example of a recent, phenotypically diverse lineage; traditional sequencing and genotyping methods have failed to detect any genetic differences between currently recognized species, despite marked variation in plumage and morphology within the genus."

Mason and Taylor write that interspecific breeding has been observed, as have birds with characteristics of two different species, though phenotypic variation has been observed to be continuous throughout the redpoll range.  But no one has been able to document significant variation in either nuclear or mitochrondrial DNA.  So, if they are genetically so similar, how is it that these birds look different enough to be considered separate species?  The authors propose three possible scenarios:

The paucity of genetic differentiation within the redpoll complex, despite marked phenotypic variation across a Holarctic distribution, could be the result of multiple evolutionary scenarios (Marthinsen et al. 2008): redpolls may be comprised of (i) a single, undifferentiated gene pool that exhibits phenotypic polymorphism, in which phenotypic differences reflect locally adapted demes or neutral phenotypic variation within a single metapopulation; (ii) multiple gene pools that have recently diverged, in which incomplete lineage sorting has hindered the capacity of previous studies to differentiate populations or species; or (iii) multiple divergent gene pools that are actively exchanging genes through hybridization and introgression via secondary contact.

They compared the niches of hoary and common redpolls and determined that hoary redpolls prefer higher latitudes while common redpolls show less of a preference and are more widespread, with much overlap.  But they don't believe that the difference was enough to explain morphological differences between the birds.  That is, geographic isolation, the usual explanation for speciation, doesn't explain the phenotypic variation observed among redpolls.

Mason and Taylor note that the lack of outlier SNPs suggests that the different redpoll species, as now recognized, share a very recent ancestry.  If there were outliers, this would suggest that the birds had had a long history of no contact, during which time genetic variants arose and spread, but then the species reunited, and the interbreeding would have dispersed much, but not all, of those variants between the entire family.  That is, option i above; this is a single undifferentiated gene pool that exhibits phenotypic polymorphism.

Intriguingly, we found novel differences in gene expression that are correlated with redpoll phenotypes, suggesting that gene expression might play an important role in generating phenotypic diversity among redpolls.

This is intriguing.  Mason and Taylor suggest that redpolls should now be considered a single species,  although as Axelson says, this is up to the American Ornithologists Union.  But, given the very low genetic diversity even between widely dispersed birds, and the fact that phenotypic variation is continuous within the genus, it makes sense.  They further suggest that gene expression differences could be due to environmental conditions which trigger phenotypic plasticity in traits like bill width or plumage coloration.

Without whole genome sequencing, these results remain suggestive.  There may be as of yet unknown regions of the genome that are responsible for the variation seen in this species, but the lack of variation in SNPs throughout the genome suggest this is probably not going so.

Evolutionary considerations and the species problem
Evolutionary biologists know that there is a 'species problem'.  That is, only individuals are clear-cut distinct natural units (and, given their colonization by bacteria and the like, even they aren't all that discrete).  Species would be next, but it is about group properties and there are many definitions.  The most commonly accepted is that a species is a group of individuals that can successfully mate and produce fertile offspring.  Similar individuals whose offspring are always sterile would be assigned different species.  Different appearance need not imply mating incompatibility (as, for example, people from Africa and Polynesia, who are inter-fertile).

Single genetic changes have been found to lead to mating incompatibility, as between populations of fruit flies.  Of course changes of any sort can do this in the case of individual human couples.  If there is mating incompatibility among groups, at least, we call them different species.  Among other reasons, the expectation is that over time they will diverge in their genes and traits, with or without the aid of natural selection, and become ever more different.  Only with shared mating would these differences be blended and circulated through a species' population.

We can note four important points here.  First, species can be defined in many ways, but the idea of genetic isolation as an enabler of separate adaptation and divergence, that goes back to Darwin, is important in accounting for the evolution of diversity.  Second, speciation is a separate phenomenon from diversity of traits.  The latter is found both within and between populations of the same species. These are obvious but subtle points, often missed or overlooked even by biologists who equate natural selection and trait differences with species differences.  Mating incompatibility enables the accumulation of trait differences, but trait differences do not in themselves enable speciation.

Thirdly, what we haven't mentioned yet, is polyphenism.  This is a well-known phenomenon in which the same genotype can yield very different phenotypes (traits) in different environments.  This can happen if something in the diet produces pigments, or it can happen if genes are expressed, or not, depending on environmental conditions, leading to environment-specific results, in different individuals with the same genotype or the same genotype in different environments.  For example, the brown goldfinches in our back yard are turning yellow as spring comes.

Fourth, individual groups whose members could physically and genetically mate successfully, but don't, either because they are isolated from each other, don't come into contact, or just simply don't do it even if they could, are sometimes considered to be different species.  Usage varies and it's a judgment call, with  no external 'law' necessitating the definition.

There is no one principle or rule about by which biological species can be defined by trait comparisons, or genomic comparisons alone.  Each case is different, and since genotypic differences  or trait differences can, but needn't indicate, species differences, one has to study each case on its own merits.  That's not always easy, but it's the nature of life.