The seeds of speciation

A red crossbill, photographed in Oregon. (Flickr: Rahul Alvares)

You don’t have to get very far into an evolution textbook before you bump into Darwin’s finches, the birds descended from South American finches that colonized the Galapagos Islands and “radiated” into an array of different species, each with a beak adapted to different food sources across the archipelago. Another, equally interesting case of avian adaptation is found in North America, on a different sort of archipelago. It’s found in patches of lodgepole pine forest that cloak the slopes and foothills of the Rocky Mountains, in the hooked beaks of red crossbills.

In the Rockies, crossbills feed on lodgepole pine seeds, using the tips of those hooked beaks to prise open the scales of seed cones. You might think that the trees would object to this, and they do, so to speak — but across most of the area where lodgepole pines face off with crossbills, they’re also under attack by an even more pernicious threat, red squirrels. Unlike crossbills, which get into pine cones while they’re attached to the tree, squirrels gnaw whole cones free from the branches, and they target larger cones, which contain more seeds. The result is that most lodgepole pine populations have evolved small, squat cones with thickened bases that protect against harvesting squirrels. However, in the South Hills of Idaho, some patches of lodgepole pine are free of squirrels — and in those sites, the pines’ cones are longer and narrower, with thickened scales at the tip, where crossbills prefer to start their prying. Those differences make an effective defense against the birds, and South Hills crossbills have evolved deeper beaks to cope.

This situation is a classic “geographic mosaic of coevolution”, a landscape of populations in which crossbills and lodgepole pine have the potential to shape each others’ evolution, but only do so in the right kind of (squirrel-free) environment. The details of the crossbill-lodgepole mosaic have been studied extensively, but it’s not been clear whether South Hills crossbills are genetically isolated by coevolution with pine in that one tile of the mosaic. If they are, the birds’ adaptation to the tree’s defenses might be setting the South Hills crossbills on the road to the origin of a new species.

A crossbill applies its crossed bill to a green seed cone. (Flickr: John Matthews)

Previous studies with relatively simple genetic markers haven’t found much genetic differentiation, and crossbills migrate long distances to follow seed crops, giving them lots of opportunities for interbreeding to break down local genetic differentiation. A paper published late last year in Molecular Ecology, however, has applied modern genetic data to that question — and it finds that there is, in fact, something different going on in the South Hills.

Collaborators at the Universities of Nevada Reno, Sheffield, and Wyoming, including crossbill specialists Craig Beckman and Thomas Parchman, used genotyping-by-sequencing to genotype more than 18,000 single-nucleotide polymorphism markers in a sample of 219 red crossbills from a number of populations distinguished by their calls and their association with different conifer species, including the South Hills birds. This much bigger, DNA sequence-based dataset replicated the prior result that there’s relatively little genetic differentiation among most of the crossbill populations, except in one case: the South Hills crossbills.

The South Hills birds form a monophyletic group within the tree of relationships among the sampled birds — that is, they’re all each other’s closest relatives. In a principal components analysis that summarizes the data from all those markers into two main axes of variation, the first axis, which accounts for the largest independent portion of the data, splits the South Hills crossbills from all the others. And in a clustering analysis, the South Hills birds break out from the rest of the dataset first, and most cleanly.

A tree of relationships among 219 crossbills from nine populations, with the South Hills birds (in red) forming a monophyletic group. Figure 1 from Parchman et al. (2016)

Even with 18,000 markers, the data presented is probably not enough to reliably find individual genes that underlie differences between the South Hills crossbills and other populations, but this confirms that they’re effectively isolated, in spite of crossbills’ nomadic lifestyle. The authors explain that the South Hills crossbills are themselves non-nomadic, and maintain a population density as high as the local, crossbill-adapted lodgepole pines will support. That puts immigrants from other crossbill populations at a particular disadvantage of intense competition for pine seeds locked up in cones that are specifically evolved to thwart them.

Using species distribution modeling for lodgepole pine and historical climate reconstructions, the authors also demonstrated that the patch of lodgepole forest in the South Hills probably wasn’t present as recently as 6,000 years ago. That means the South Hills crossbills started their evolutionary path away from the rest of the species very recently by geological standards, adapting on the same time-scale as classic cases of rapid evolutionary change like the lizards of White Sands, New Mexico — and quite a bit faster than Darwin’s finches.

References

Benkman CW. 2003. Divergent selection drives the adaptive radiation of crossbills. Evolution. 57(5): 1176-1181. doi: 10.1554/0014-3820(2003)057[1176:DSDTAR]2.0.CO;2

Benkman CW, TL Parchman, A Favis, and AM Siepielski. 2003. Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. The American Naturalist 162(2): 182-194. doi: 10.1086/376580

Edelaar, P and CW Benkman. 2006. Replicated population divergence caused by localized coevolution? A test of three hypotheses in the red crossbill-lodgepole pine system. Journal of Evolutionary Biology, 19: 1651–1659. doi: 10.1111/j.1420-9101.2006.01113.x

Parchman, TL, CW Benkman, and SC 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, TL, CA Buerkle, V Soria-Carrasco, and CW Benkman. 2016. Genome divergence and diversification within a geographic mosaic of coevolution. Molecular Ecology, 25: 5705–5718. doi: 10.1111/mec.13825

Thompson, JN. 2016. Coevolution, local adaptation and ecological speciation. Molecular Ecology, 25: 5608–5610. doi: 10.1111/mec.13873

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About Jeremy Yoder

Jeremy Yoder is an Assistant Professor of Biology at California State University, Northridge. He also blogs at Denim and Tweed, and tweets under the handle @jbyoder.
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