Genomic Islands of Speciation… are real?

I really want genomic islands of speciation to be real. Those great studies that seemed so convincing over the last ~10 years have been squashed due to, among other things, the trickiness of low genetic diversity (stay with me, I’ll elaborate below). But conceptually, genomic islands just have* to be real. Luckily, a recent paper by Marques et al., has given me hope.
What’s a genomic island of speciation?
We can imagine two sympatric populations that are divergent due to local adaptation or reproductive isolation. However, many such populations (or species) still experience gene flow. Genomic islands of speciation (also known as genomic islands of divergence) are the parts of the genome that underlie this reproductive isolation or adaptation and are resistant to the homogenizing effects of gene flow. These regions are what make the populations distinct and they stand out in contrast to the rest of the genome, which should be homogenized due to gene flow. To me, this idea is appealing because it helps explain how rampant fine scale local adaptation persists in the face of gene flow and can lead to ecological speciation.
But do they actually exist?
Proving the existence of genomic islands has been much trickier than anticipated. Cruickshank and Hahn’s (2014) re-analysis of five data sets previously thought to demonstrate genomic islands found that all of the identified regions had low genetic diversity, which gave the false appearance of high divergence and low gene flow**; the regions weren’t real outliers. Moreover, heterogenous divergence across the genome can also occur under scenarios of allopatric speciation, which, of course, isn’t caused by variation in gene flow across the genome but rather because of drift, selection, varying recombination rates, etc. (for a discussion, see Noor and Bennett 2009). This calls into question the role of genomic islands in scenarios of divergence with gene flow and really makes you wonder if they exist at all.
Just kidding, they probably exist
Marques and co-authors take a clever approach to test for the presence of genomic islands. They used a system of stickleback that was established only 150 years ago but has since diverged into stream and lake ecotypes. In one stream, lake and steam populations breed sympatrically because lake individuals move into the stream to spawn. The second stream is longer and lake individuals can’t make it far enough upstream to breed sympatrically (at least, not in one generation), resulting in a parapatric stream population.


Sampling locations. From Marques et al. 2016.

This paired system allows the authors to test expectations of ecological speciation with gene flow. For example, they expect to observe parallel divergence for both the stream populations, but also predict:

…to the extent that speciation is constrained by gene flow, we expect lower average genomic differentiation, a smaller number of islands of differentiation and less heterogeneity in genomic differentiation in the sympatric than in the parapatric contrast.

Using RADseq, all both steam populations were compared to the lake population. General divergence between the populations matched expectations; the sympatric population was less divergent from the lake population than the parapatric population. They then looked for islands of divergence between the populations pairs and found 37 island regions. 19 of these showed parallel changes in the stream populations compared to the lake populations and were generally clustered on a few chromosomes (see figure). Perhaps most importantly, they showed that the island regions did not have lower genetic diversity than the rest of the genome!


Overview of the genomic islands of speciation that were identified. From Marques et al. 2016

While it is easy to be skeptical of studies claiming to find genomic islands of speciation, Marques et al. provide quite a convincing argument. And while I don’t know if genomic islands are prevalent, I now have more faith that they’re real.
*I suppose they don’t have to be real. But really, it seems like they should be.
**This is why you should always use absolute measures of divergence instead of relative measures.
Cruickshank, Tami E., and Matthew W. Hahn. “Reanalysis suggests that genomic islands of speciation are due to reduced diversity, not reduced gene flow.” Molecular ecology 23.13 (2014): 3133-3157.
Marques, David A., et al. “Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback.” PLoS Genet 12.2 (2016): e1005887.
Noor, Mohamed AF, and Sarah M. Bennett. “Islands of speciation or mirages in the desert? Examining the role of restricted recombination in maintaining species.” Heredity 103.6 (2009): 439-444.

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