Fishing for Speciation Genes

Let’s face it – speciation is a complex process, wrought with numerous “small-pieces-of-the-puzzle” that have had scientists brawling and losing sleep over for a century. Darwin was perhaps right (again) when he wrote:

… I look at the term species, as one arbitrarily given for the sake of convenience to a set of individuals closely resembling each other, and that it does not essentially differ from the term variety, which is given to less distinct and more fluctuating forms. The term variety, again, in comparison with mere individual differences, is also applied arbitrarily, and for mere convenience sake.

While species definitions themselves are rather fuzzy, one might question the validity of arguing for the presence of so called “speciation” genes in the absence of reproductive incompatibility, or inviable hybrids. A general view of speciation involving a “continuum” – in space and time, where populations are continually evolving adaptively in response to natural selection is perhaps more acceptable (see Hey 2001 for a detailed account of the species problem), but we will save that for a later discussion, and focus on “speciation” genes instead. Wu and Ting (2004) define these genes as “…(genes) which are important in driving the nascent species to become independent genetic entities”, supported by Orr et al. (2004) in delineating these genes as instrumental in producing, and maintaining hybrid sterility or inviability. Specifically, Nosil and Schluter (2011) call them as “…those genes whose divergence made a significant contribution to the evolution of reproductive isolation between populations.” (also see Table 1 of Nosil and Schluter for a list of alternate definitions). They also set forth three criteria for identifying these speciation genes – (1) demonstrating its effect on reproductive isolation, (2) divergence at the gene occurred prior to completion of speciation, and (3) quantifying the effect size of the gene in increasing reproductive isolation.

Is reproductive isolation a pretext for speciation? Image courtesy: http://evolution.berkeley.edu/evolibrary/article/evo_44

If we remove the pretext of complete reproductive isolation (or apparent lack of gene flow, or viable/fertile hybrids), perhaps a more general definition would allow for speciation with gene flow (continuum), where divergent selection (and subsequent hitchhiking or sweep) is exacerbated at these so called speciation genes (or islands/continents – see Feder et al. 2012). Interestingly, regardless of the “phase” of speciation in the system, speciation genes/islands/continents (I’ll call them loci hereon for generality) share some commonalities in their footprints on extant genomes – they exhibit reduced variation compared to the rest of the genome, often easily detected using summary statistics like F_st, D_xy, φ_st, etc. However, the source of this reduced variation is cause for yet another long-standing debate – is reduction in variation due to reduced gene flow at speciation loci, and subsequent divergent selection, or due to linked selection (background selection or hitchhiking) at speciation loci?

Mullerian mimicry in Heliconius butterflies – examples of speciation in the face of gene flow. Image courtesy: Repeating Patterns of Mimicry. Meyer A, PLoS Biology, Vol. 4/10/2006, e341 doi:10.1371/journal.pbio.0040341

Several recent publications have pointed to this difficult issue (see Cruickshank and Hahn 2014 for a review). So at the heart of the problem of identifying speciation loci is a second problem – one of decoupling the effects of differential migration and selection. Both ideas have substantial empirical support. For example, Burri et al. (2015) describe the dominating effects of lineage-specific diversification in flycatchers (Ficedula), versus gene flow using a massive genomic data set, Feulner et al. (2015) describe equally compatible models of differential gene flow, and linked selection in shaping genomic diversity in lake and riverine populations of three-spine sticklebacks (Gasterosteus aculeatus), whereas Supple et al. (2015) compare genomic divergence levels between hybridizing and non-hybridizing species of Heliconius butterflies, to describe the role of differential gene flow, and genomic hitchiking in incipient speciation. A common denominator however, for both concepts, is population demography. For instance, reduced gene flow might as well be due to small population sizes, and not necessarily due to diversifying selection at speciation loci. Similarly, small populations have reduced efficacy of linked selection, easily contributing to “noisy” speciation loci while fishing for reduced diversity. Perhaps the bigger problem thence is quantifying the effects of demography in contributing to reduction in genomic diversity, getting at which will take us one step closer to identifying speciation genes.

On a related subject, see Yaniv’s fun account of a clash of minds on speciation-with-gene-flow versus speciation-and-gene-flow.

References

Burri, Reto, et al. “Linked selection and recombination rate variation drive the evolution of the genomic landscape of differentiation across the speciation continuum of Ficedula flycatchers.” Genome research (2015).

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.

Darwin, Charles. “On the origin of species.” Murray, London 360 (1859).

Feder, Jeffrey L., Scott P. Egan, and Patrik Nosil. “The genomics of speciation-with-gene-flow.” Trends in Genetics 28.7 (2012): 342-350.

Feulner, Philine GD, et al. “Genomics of divergence along a continuum of parapatric population differentiation.” PLoS Genet 11.2 (2015): e1004966.

Hey, Jody. Genes, Categories, and Species: The Evolutionary and Cognitive Cause of the Species Problem: The Evolutionary and Cognitive Cause of the Species Problem. Oxford University Press, 2001.

Nosil, Patrik, and Dolph Schluter. “The genes underlying the process of speciation.” Trends in Ecology & Evolution 26.4 (2011): 160-167.

Orr, H. Allen, John P. Masly, and Daven C. Presgraves. “Speciation genes.”Current opinion in genetics & development 14.6 (2004): 675-679.

Supple, Megan A., et al. “Divergence with gene flow across a speciation continuum of Heliconius butterflies.” BMC evolutionary biology 15.1 (2015): 204.

Wu, Chung-I., and Chau-Ti Ting. “Genes and speciation.” Nature Reviews Genetics 5.2 (2004): 114-122.