Is prezygotic isolation more important than postzygotic isolation at the onset of speciation?

A simulation study casts doubt on this common statement.

“Ethological barriers to random mating constitute the largest and most important class of isolating mechanisms in animals.” If you like bold, in-your-face proclamations, you can always turn to the work of German biologist Ernst Mayr. He never shied away from strong statements, such as the one at the start of this blog post. In his book Animal Species and Evolution, he argued that speciation in animals usually begins with behavioral differences. Members from different populations prefer familiar faces and rarely interbreed. This behavior – assortative mating – generates a first genetic barrier between the populations. Later in the speciation process, selection against the occasional hybrid can arise in the form of sterility or unviability.

To put this argument in the modern jargon of speciation research: prezygotic isolation is more important than postzygotic isolation in the initial stages of speciation. If you are not familiar with these terms, I will briefly define them. Luckily, I can quote from the introduction of my PhD thesis for a concise explanation.

Prezygotic isolation mechanisms act before fertilization, whereas postzygotic isolation mechanisms act after fertilization and can be either intrinsic or extrinsic. Intrinsic postzygotic isolation mechanisms lead to sterility or unviability of the offspring, while extrinsic postzygotic isolation mechanisms encompass lower fitness of the offspring for ecological or behavioral reasons, not developmental defects.

The idea that prezygotic isolation is more important than postzygotic isolation makes intuitive sense. First, there is a reduction in gene flow between populations due to behavioral differences. Next, the populations follow different evolutionary paths and accumulate genetic incompatibilities. When the populations establish secondary contact, potential hybrids are sterile or unviable due to the many genetic mismatches. Makes sense, right? But if there is one thing I have learned during my short scientific career, it is to be careful with intuitive ideas. Evolutionary biology is often counterintuitive.

 

Simulating Clines

A recent study in the journal The American Naturalist put this idea to the test. Darren Irwin performed some simulations comparing different levels of assortative mating and postzygotic isolation (i.e. hybrid fitness). To assess the impact of these processes on speciation, he turned to cline theory. Loyal readers of this blog might be familiar with this mathematical framework, but to get everyone on the same page I will outline the main concepts of cline theory (based on a previous blog post).

Let’s say you have a white species and a black species that produce gray offspring in a hybrid zone. You observe birds along a transect and note down their plumage color. When you put the data in the graph, you will see a transition from white birds (when you were in the habitat of the white birds) through grayish birds (in the hybrid zone) to black birds (in the black bird habitat). The useful aspect of cline theory is that the shape of a cline can tell you something about the biology of the birds. For example, if the gray hybrids interbreed with their parental species, there will be a variety of backcrosses of different colors. Some more white and some more black, depending on the species they crossed with. This will result in a smooth transition from white through different (perhaps 50) shades of gray to black. In other words, a wide cline. However, if gray birds cannot find a mate, there will be mostly gray hybrids in the contact zone. This will result in a rapid transition from white to black plumage, a steep cline.

Darren Irwin applied this approach to his simulations. A wide transition with many backcrosses indicates that reproductive isolation is weak and there will be gene flow between the pure populations. A steep cline, however, points to strong reproductive isolation. What kind of cline does assortative mating produce?

An example of a cline plot. There are only white birds to the left of the hybrid zone and black ones on the right side. In the hybrid zone there are different shades of gray birds.

 

Genetic Bridge

Let’s start by comparing two simple scenarios: (1) modest selection against hybrids (10% reduction in hybrid fitness) and (2) modest assortative mating (female is 10 times more likely to pick a partner from her own species). Running the first scenario produces a steep cline because hybrids are less fit than their parents and rarely backcross. This result confirms the so-called tension zone model that was described by Nick Barton and Godfrey Hewitt in the 1980s. The narrow hybrid zone is maintained by a balance between pure individuals moving into the contact zone and selection against unfit hybrids.

The second model – with modest assortative mating – produces a much wider cline. Because there is no selection against hybrids, they can interbreed with each other and their parental species. These dynamics result in a variety of hybrids and backcrosses that form a genetic bridge between the initial parental populations. If gene flow is sufficiently high, the two populations might even merge into one large population.

The outcomes of simulating hybrid zone dynamics. A reduction in hybrid fitness (i.e. postzygotic isolation) results in a steep cline (in green), while modest assortative mating produces a wide cline (in purple). Adapted from: Irwin (2020) The American Naturalist

 

Search Costs

These initial findings indicate that modest assortative mating cannot jumpstart speciation. However, further analyses uncovered some conditions in which assortative mating leads to a narrow, steep cline, namely (1) when assortative mating is encoded by a single locus, (2) when assortative mating is very strong, and (3) when the cost of searching for a mate is high.

The first condition – assortative mating is encoded by a single locus – is not very realistic. Genomic studies have shown that reproductive isolation is mostly encoded by multiple genes (but see this case of single gene speciation in snails). The other two conditions – strong assortative mating and high mate searching cost – are actually a form of postzygotic isolation because they impact the mating chances of hybrids. Indeed, if assortative mating of the parental populations is strong, the hybrids won’t be able to find a mate.

The effect of search time is more complex. In the simulations, search time was modelled as the cost a female pays when she rejects a potential mate. A high search cost thus leads to females that quickly choose a mate. This is at the disadvantage of hybrids because they are rare in the population. In addition, hybrid females in the center of the hybrid zone will most likely mate with other hybrids. This lowers the likelihood of backcrossing with the parental populations and the consequent formation of a genetic bridge.

Results of simulations with and without mate search costs. Each graph shows the relationship between assortative mating (on the x-axis) and hybrid fitness (on the y-axis). The colors indicate the width of the cline (on the left) and the probability of a bimodal hybrid zone (i.e. two distinct populations, on the right). Including mate search costs leads to narrower clines (more yellow in the left figure) and a higher probability of distinct populations (more yellow in the right figure).

 

Postzygotic Isolation

These simulations suggest that assortative mating is less important in speciation than we think. But it’s just a modelling exercise, some of you might say. How realistic are these results? Well, several studies have tried to estimate the strength of assortative mating in wild populations. The highest estimate by Christophe Randler – based on 58 avian hybrid zone studies – points to  an assortative mating strength of 2.6. This is considerable lower than the modest strength of 10 used in the simulations. Of course, this strength might vary between hybrid zones, but it seems that assortative mating is rarely strong enough to keep populations separate.

This study thus indicates that assortative mating on its own cannot prevent populations from merging, some form of postzygotic isolation is needed (e.g., lower mating chances for hybrids). The intuitive idea that “prezygotic isolation is more important than postzygotic isolation” does not hold here. Why did this statement become so popular? The main reason is probably the focus on extreme forms of postzygotic isolation (i.e. hybrid sterility and unviability) that take long to evolve. We should not forget other postzygotic isolation mechanisms, such as sexual selection against hybrids. This insight opens up new research opportunities, nicely summarized at the end of the paper: “While assortative mating, unless perfect or very nearly so, is ineffective on its own in maintaining isolation of two species, the effects of sexual selection and sexual signals on postzygotic isolation are likely strong and worthy of renewed research focus.”

 

References

Irwin, D. E. (2020). Assortative mating in hybrid zones is remarkably ineffective in promoting speciation. The American Naturalist, 195(6), E150-E167.

Featured image © Zorba the Geek | CC-BY-SA-2.0 Wikimedia Commons

 

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