Noor and Feder Review the Genetics of Speciation

Nature Reviews Genetics has published a review (go figure) of speciation genetics penned by Mohamed Noor and Jeff Feder. Here is the purpose of the review, from the horses' mouths:

Here, we review how recent advances in molecular and genomic techniques are helping to achieve a greater understanding of the genetics of speciation. For the purpose of this review, we focus on technical advances rather than theoretical concepts, which are discussed extensively elsewhere. We define speciation for sexually reproducing organisms as the transformation of within-population variation into taxonomic differences through the evolution of inherent barriers to gene flow. This definition is not universally accepted, but it remains the most commonly used by students of speciation and is of the greatest utility to dissecting the genetics of the process. We discuss whether and how molecular techniques are helping to discern the genetic bases and evolutionary origins of barriers that contribute to population divergence. We present some recent discoveries from laboratory and field studies that apply molecular and genomics techniques to the speciation question.

The "elsewhere" they cite is Coyne and Orr's Speciation, which they describe as "a rigorous, authoritative and provocative review of the entire field of speciation." I like that description. Noor and Feder start with the work of Mayr and Dobzhansky and work their way to the post-genomic era. Here are a few highlights from the review:

• Choice quote: "Despite the dramatic advances in molecular and genomic techniques, the 'old-school' approaches of Dobzhansky and Mayr for studying the genetics of speciation still apply today." Okay, I only like it 'cause they refer to Teddy D. and Ernst as old-school. If they were alive to defend themselves, dudes would get nu skool on yo' ass.

• They point out a divide in the speciation community between researches who work on model organisms in the lab and those that study very recently diverged populations. Here's how they describe the model organism guys:

  At one extreme are the researchers who investigate barriers to gene flow using laboratory crosses of well-established model species, often focusing on easily scored phenotypes such as hybrid sterility or inviability. They have been successful in identifying genes that contribute to these traits (see below). However, the specific traits or genes identified might not directly reduce or have previously restricted gene flow between the focal species in nature (indeed, they often do not, as several species studied in this way do not occur together in nature). Moreover, these genes could contribute to reproductive isolation in the laboratory, but if they arose after gene flow was essentially complete between species in nature, they would not represent 'speciation' loci in the strict sense. Nonetheless, these studies have provided valuable genetic and evolutionary insights that can be applied to naturally hybridizing but less tractable species, and have identified the rate of accumulation of alleles that cause hybrid incompatibilities in isolated species.

  And here are the people that work on hybridizing populations:

  At the other extreme are naturalists who study very recently diverged, often hybridizing populations. Although their studies are directly applicable to natural divergence in its early stages, the populations might be ephemeral and never actually speciate: such taxa could eventually fuse. So, an unproven assumption of eventual speciation underlies these studies.

  As evidence for diverging populations that fail to speciate, they cite this paper on sticklebacks, which I wrote about here (and John Hawks wrote about here). Noor and Feder end on a very diplomatic note, saying that "complementary insights are yielded by these two approaches."

• On interpreting molecular data:

  Genetic data alone do not answer the question of whether taxa are or have undergone introgressive hybridization unless the results are viewed in the context of an appropriate evolutionary model for rigorous statistical testing. Concomitant with the advances in technology, more sophisticated analytical methods are also being developed to discern whether shared variation is due to introgression from a related species or represents the persistence of ancestral polymorphism. These methods can be categorized as being based on either summary population genetic statistics or phylogenetic gene-tree-building approaches. Gene-tree approaches can reveal alleles that show discordant phylogenetic patterns (paraphyly) that could indicate introgression, but could also be explained by incomplete lineage sorting. Gene trees have also been used to distinguish historical processes through nested clade analysis. However, because it is difficult to devise powerful statistical tests of competing hypotheses for gene-tree-based methodologies such as nested clade analysis, one can incorrectly accept a best-fit model for a process that never occurred. So, gene trees could find their most practical application as a first, qualitative approach to identify loci that might have introgressed in the past or to identify taxa of possible hybrid origin.

• Inversions are important for preventing introgression between hybridizing species/populations. These regions contain genes responsible for the phenotypic divergence between populations. But that's hardly a surprise coming from these two guys.

• Here's an example where they echo a point that is dear to my heart:

  Most studies have examined genetic divergence either across the genome using the single genome sequence assemblies for each species . . . or using multiple individuals of each species but typically only 30 or fewer loci . . . The former gives a genome-wide view but lacks the ability to distinguish divergence from polymorphism within species, whereas the opposite is true for the latter approach.

  This is pretty much true of the entire field of evolutionary genetics, not just research on speciation. Use the available data (ie, whole genomes) to guide your research, but always test your hypotheses using some secondary data (polymorphism, expression, experimental analysis). As we become more and more high-throughput it will be easier to perform these secondary analyses.

• From the conclusion: Do not neglect non-model organisms, which is interesting coming from two guys who work on speciation models (Drosophila sister species and Rhagoletis). We've reached a point where we can generate data faster than it can be analyzed. The high-throughput analyses are great for producing hypotheses, but they must be tested using "careful and precise old-school reductionist bench work" (yes, that's two instances of 'old-school' in the paper). Finally, they suggest that we may be able to sort out the order in which isolation events occurred for particular speciation events. Additionally, by comparing independent speciation events, we may observe trends regarding the order in which different barriers to gene flow emerge.

• And for those people interested in species concepts, here's the last sentence of the paper: "One day we might even reach consensus on the nagging question of what exactly constitutes a species." I, of course, already know the answer. A species is whatever you want it to be so that you can study what you deem to be speciation.