I’ve been chatting up Wilkins about the role of natural selection in speciation (and when I say “speciation” I mean “reproductive isolation”). Wilkins listed a few cases where speciation would occur independently of natural selection. Amongst the mechanisms in Wilkins’s list was speciation via karyotypic changes (polyploidy, inversions, fusions or fissions). I cried shenanigans, and this is why.
The karyotype refers to the organization of an organism’s genome — chromosome number, fusions/fissions of chromosomes, and gene order within chromosomes. One way to change the karyotype is to duplicate the entire genome (tetraploidization), which often results in reproductive incompatibilities between the tetraploid individuals and the diploid (normal) individuals. If the tetraploid individuals do find a way to reproduce (either by selfing, finding another tetraploid individual, or mating successfully with a diploid individual), there’s a good chance that the new karyotype (the tetraploids) will be reproductively isolated from the diploids. In this case, the karyotypic mutation itself has led to reproductive isolation without natural selection acting on any other variation.
But what about other karyotypic changes? Do they result in “instantaneous” reproductive isolation?
As I have mentioned before, chromosomal fusions and fissions do not, in and of themselves, prevent matings between individuals with different karyotypes. Individuals with fused chromosomes should be able to successfully mate with individuals with unfused chromosomes producing heterokaryotypic progeny. Unlike the case with polyploidy, fusions and fissions do not induce instantaneous reproductive isolation.
But what I’m more interested in are chromosomal inversions. The meiotic effects of these karyotypic rearrangements are better studied than fusions and fissions. We also know about a lot of examples of inversions segregating within natural populations. It was once hypothesized that inversions could induce instantaneous speciation much like polyploidy can. But the fitness costs of carrying two different arrangements differentiated by an inversion are too low; this is inferred based on the amount of inversions segregating in natural populations.
Here’s the twist: inversions can and do play a role in speciation, and it’s in conjunction with natural selection (ie, Wilkins was wrong). Rather than acting as an intrinsic cause of reproductive isolation, inversions are the substrate upon which the causes of reproductive isolation arise and evolve. That’s a mouthful and rather unintelligible without the details, some of which I’ll provide for you below. Keep in mind that it’s not the inversions themselves that allow for reproductive isolation, but without them speciation would proceed much more slowly.
First, let’s lay out our assumptions. We will assume that two populations have diverged to some extent such that interpopulation hybrids (individuals produced by matings between individuals from different populations) are less fit than progeny produced by intrapopulation matings (we call this “post-zygotic isolation”). It follows that natural selection will favor pre-zygotic isolating barriers (ie, prior to the fusion of egg and sperm) between the populations to prevent the production of interpopulation hybrids. If the populations are not entirely isolated (they come in contact and can mate with each other) these barriers must be behavioral, and, if they are to be acted on by natural selection, must be heritable (ie, genetic).
Given that there is some gene flow between the populations, the genetic factors for prezygotic reproductive isolation within one population could be transmitted to the other population during the interpopulation matings that occur. Individuals carrying the alleles that prevent them from mating with the other population are more fit (because their progeny are more fit), but if those alleles move between populations due to interpopulation hybridization, the alleles will not be as effective at preventing interpopulation hybridization. How can the movement (or migration) of the alleles from within one population into the other be prevented? This is where inversions fit in.
Inversions suppress recombination in heterokaryotypic individuals. An individual with two different versions of a particular chromosome (they are differentiated by at least one inversion) tends to produce gametes with very few crossing over events along that chromosome (all the alleles within the inversion are tied together). Now, imagine our two populations not only have some postzygotic isolating barriers between them, but are also karyotypically differentiated by at least one inversion on at least one chromosome. The inversion does not prevent interpopulation hybrids, but what if the genes for reproductive isolation are located with the inversion? Rather than being transmitted as single, independent alleles between populations, they are locked within the inversion and must be transmitted as a unified group.
A similar scenario has been modeled by Navarro and Barton, and they found that inversions significantly accelerate the accumulation of postzygotic isolating barriers between populations. It’s not the inversions themselves that lead to reproductive isolation; it’s the genes contained with the inversions. Gene flow between the populations is drastically suppressed within the inverted regions because the inversions contain genes that decrease fitness in interpopulation hybrids, and they are transmitted as a block because of the inversion. And natural selection can act on the genes within the inverted regions because they either confer some intrinsic fitness benefit or they favor reproductive isolation between the populations.
Not only does the model work out well on paper, the model was tested by Mohamed Noor’s lab using the model organisms from the Drosophila pseudoobscura subgroup. Noor’s group mapped hybrid male sterility factors (genes that decrease fertility in interspecific hybrid males) between two species pairs. The first pair, D. pseudoobscura and D. persimilis, have overlapping ranges in the northwestern United States, while the second pair, D.p. bogotana and D. persimilis, do not (D.p. bogotana is located in northwestern South America, in and around Bogota, Columbia).
Navarro and Barton’s model predicts that gene flow between populations will lead to genes for reproductive isolation mapping to within inverted regions. It makes no such predictions when there is no gene flow between populations. Consistent with the model, the hybrid male sterility factors between D. pseudoobscura and D. persimilis (the species pair with overlapping ranges) map to regions of the genome which contain inversions that differentiate the two species. In the non-overlapping species pair (D.p. bogotana and D. persimilis), the genes show no preference for inverted regions.
Additionally, there is some evidence that inversions may play a role in the reproductive isolation of a classic model organism in speciation research: Rhagoletis pomonella. These fruit flies appear to be speciating due to the recent introduction of cultivated apples into North America. Prior to the introduction of apples, the flies fed, mated, and laid their eggs primarily on hawthorns (another fruit), but they can now be found on both plants. The two plants fruit at different points in the season, and this has led to two separate host races that each prefer one fruit over the other. Jeff Feder and colleagues mapped loci for host plant preference and found evidence that they mapped to within inverted regions (identifying inversions in Rhagotelis is much more difficult than in Drosophila). They have also hypothesized that the inversions (and possibly the genes that predisposed the species for a speciation event) were introduced into the population via individuals migrating in from Mexico.
In these examples, the inversions themselves are not under natural selection and do not induce speciation. But the genes contained within are responsible for traits involved in pre- and post-zygotic reproductive isolation between populations. It’s these genes that are under selection and responsible for the evolution of reproductive isolation (speciation). Therefore, to say that speciation via karyotypic mutations proceeds without selection is misleading. Yes, polyploid speciation occurs via the intrinsic reproductive isolation of tetraploids from diploids, but inversions play a much more intricate role in the speciation process, in concert with genes responsible for reproductive isolation and selection acting upon those genes.
Brown KM, Burk LM, Henagan LM, Noor MAF. 2004. A test of the chromosomal rearrangement model of speciation in Drosophila pseudoobscura. Evolution 50:1856-1860. doi:10.1554/04-174
Feder JL, Berlocher SH, Roethele JB, Dambroski H, Smith JJ, Perry WL, Gavrilovic V, Filchak KE, Rull J, Aluja M. 2003. Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proc. Natl. Acad. Sci. USA 100:10314-10319. LINK
Feder JL, Roethele JB, Filchak K, Niedbalski J, Romero-Severson J. 2003. Evidence for Inversion Polymorphism Related to Sympatric Host Race Formation in the Apple Maggot Fly, Rhagoletis pomonella. Genetics 163:939-953. LINK
Navarro A and Barton NH. 2003. Accumulating postzygotic isolation genes in parapatry: a new twist on chromosomal speciation. Evolution 57:447-459. doi:0014-3820(2003)057[0447:APIGIP]2.0.CO;2