Note: This series of posts is intended as a basic introduction to the science of evolution for non-specialists. You can see the introduction to this series here. In this post we examine the details of how allele flow became (mostly) blocked between two very recently diverged populations/species as they exploited different niches in the same geographic area.
In yesterday’s post, we introduced the idea that species can form in the same geographic location based on resource partitioning—where the two populations become increasingly suited, over time, to exploit different niches. In this post, we’ll explore this phenomenon in detail, using an example of nascent species that have formed in the very recent past, and under human observation: diversification within hawthorn flies, Rhagoletis pomonella. These flies are attracted to the unripened fruits of hawthorns, a wild relative of domestic apples (i.e. something resembling a small crabapple). Hawthorn fruit is also where hawthorn flies find their mates and lay their eggs, to allow the larvae to feed on the fruit (and cause it to spoil and fall early, with the larvae along for the ride). Hawthorn flies produce only one generation per year, and survive the winter buried as pupae. Moreover, they have a short adult lifespan, giving them only a short period to find a mate, breed, and for the females to lay eggs. This crucial period, of course, is set by the life cycle of the hawthorn—when its fruit is available for the flies to use as a food source and meeting location. As such, natural selection (exerted by the hawthorn life cycle) acts on genetic variation relevant to hatching time in hawthorn fly populations. The timing of hatching shows heritable variation, and flies that happen to hatch near the fringes of when hawthorn fruit is available (or worse, when there is no fruit available at all) do not reproduce as successfully as do flies that hatch when hawthorn fruit is abundant. Not surprisingly, the result is that we observe populations of hawthorn flies that are well-timed with their host plants, with most members of any fly population hatching in concert with the height of fruit availability:
Hatching time is an example of a continuous trait, in contrast to a discontinuous trait. Discontinuous traits are traits that have distinct categories: black versus blue eyes, or red versus white flowers, and so on. Many traits cannot be “binned” into such categories, but rather form a distribution in populations. Traits such as height and weight are examples of continuous traits, and the timing of hawthorn fly hatching is another. The effect that the hawthorn tree has on the hawthorn fly is an example of stabilizing selection—fruit availability is selecting against flies that fall outside the boundaries on either side (i.e. flies hatching too early, or flies hatching too late). The overall effect is to keep fly hatching matched to fruit availability, generation after generation.
Tempted by an apple
Something happened to upset this stable, balanced interaction, however: the introduction of domestic apples to North America by European colonists. As we noted above, hawthorns and apples are related plants, with somewhat similar fruits. One difference, however, was the timing of fruit development in apples compared to hawthorns: domestic apples produce fruit some weeks earlier than do hawthorns. The introduction of apples into the hawthorn fly habitat thus provided a potential food source for flies that happened to hatch on the “early” end of the spectrum:
For those “early” flies that were attracted to this new, but somewhat similar fruit in their environment, the result would be twofold: (a) finding a food source with reduced competition from members of their own species, and (b) finding a mate with similar tendencies of attraction to apples. What was previously a “losing” genetic combination (hatching too early, without sufficient food or reasonable prospects for a mate) was now a “winning” combination. As a result, “early” variants could now reproduce much more effectively than they could before, and thus increase in number over successive generations:
In other words, once apples were present, the environment was no longer selecting fly populations in a stabilizing way, but rather acting to shape variation into two subpopulations. The selection had now switched to being diversifying selection. Importantly, these two subpopulations were not diversifying only with respect to hatching time and food preference, but also (given the nature of their biology) with respect to mating preference. As the “apple” variants increased in number, they naturally bred more frequently with other “apple” variants, since they encountered their mates on apple trees. The result was a partial barrier to allele flow that would reinforce the nascent differences between the two groups over time.
While the hawthorn and apple “species” of Rhagoletis pomonella have been the subject of human interest for centuries (mostly owing to the economic impact of the apple species as a pest) geneticists are just starting to get a handle on the allele differences that were the targets of selection during the separation process. Not surprisingly, genes known from prior research to affect hatch timing show up as having different alleles in the two groups. Other candidate genes include the receptor proteins the flies use to detect odors from their target fruits—with certain alleles more tuned to apple odors, and other alleles tuned to hawthorn odors. What started out as variation within one population has now been partitioned by selection into allele combinations suited to distinct niches—and given the short timeframe in which the switch to apples occurred, it is likely that new mutations did not play a role. Rather, recombination and segregation of existing alleles of numerous genes was enough to provide genetic differences that suited some members of the original population to exploit the new opportunity. The net effect was the shifting of a few continuous traits (hatch timing, fruit odor preference) to match a new environmental niche and precipitate a barrier to allele flow.
Selection for the few
Having considered the genes (and their alleles) that were under selection during this speciation event, there are a few points to make. The number of genes under selection (and thus with different alleles in the two new species) will be relatively rare. Only alleles that affect traits relevant to adaptation to the new niche will be affected. Most genes will remain identical between the two populations, since they were not under diversifying selection, but continued to be under stabilizing selection for their (identical) role in both species. For example, consider genes required for cellular energy conversion or wing development—processes that both species still need to do in the exact same way. These genes will have the same alleles (or perhaps only one allele) in both populations, since the function of these genes were not relevant to adapting to the new niche. In short, the overall pattern that speciation produces will be a small smattering of differences in alleles for the genes under selection (or genes that happened to experience drift by chance) against a backdrop of the large majority of identical genes that were not subject to selection (or drift).
Indeed, one reason we can be confident that the hawthorn and apple “specialists” of Rhagoletis pomonella are in fact the products of a recent speciation event (aside from the fact that farmers observed them as they arose) is because of the overwhelming identity between their genomes—they have only tiny differences in a handful of genes. Biologically, it’s an open question if they are in fact truly separate species, since they do continue to exchange alleles, albeit at a greatly reduced rate compared to sharing alleles within their respective populations. As we have seen for ring species, this example shows us that it is possible to observe in the present day the precise features we would predict for an ongoing, “in process” speciation event. Additionally, it shows that only a small handful of differences, derived from variation already existing within a population, can start two subpopulations on a trajectory that gradually improves the barrier to allele flow between them. Over time, these effects can lead to the formation of closely related species.
In the long run
The production of closely-related species from a common ancestral population is hardly controversial among evangelical Christians, though the mechanisms underlying such events are not commonly appreciated. What is more controversial for many, however, is the suggestion that these mechanisms also produce widely diverged species over greater spans of time. In the next post in this series, we’ll turn to some lines of evidence that support the hypothesis that highly diverse modern species are indeed derived from common ancestral populations deep in the past.
For further reading:
Schwarz, D. et al., (2009). Sympatric ecological speciation meets pyrosequencing: sampling the transcriptome of the apple maggot Rhagoletis pomonella. BMC Genomics 10; 633. (http://www.biomedcentral.com/1471-2164/10/633)