En garde! Assortative mating in hybrid swordtails

Understanding reproductive isolation is a pretty darn important part of understanding evolution. For new species to form, gene flow needs to be limited in some way. Under allopatry, limiting gene flow is straight forward; individuals never encounter each other so there is no opportunity to interbreed. However, when individuals can access each other this process becomes more complicated. Premating isolation is one mechanism that can limit gene flow between populations or incipient species. For example, when there is selection against hybrids, premating isolation should evolve through reinforcement.
However, premating isolation is not necessarily consistent across space and time within a species. A study led by Molly Schumer focuses on the dynamics of assortative mating in recently established hybrid populations of swordtails, Xiphophorus. In short, it’s complicated and depends on many things.
Swordtails are a great evolutionary system. These are little fish that live in streams of Central America and Mexico. Two species, X. birchmanni and X. malinche, historically have not hybridized. However, around 1997, hybrids were identified (Rosenthal et al., 2003). In certain sites, only hybrids can be found, suggesting that species recognition has somehow broken down. Further studies showed that pollution in the form of sewage and agricultural runoff disrupt chemical signaling, thus inhibiting assortative mating (Fisher et al., 2006). As a result, we know when hybridization started between species, which provides a powerful system to understand the effects of admixture on reproductive isolation.

To understand how assortative mating has change over time, Schumer and colleagues sampled 642 adults from three different locations over a 10 year time period and genotyped these individuals at 1.3 million ancestry informative sites. Of these three sites, two (Tlatemaco and Totonicapa) show the expected hybrid swarm. The third, Aguazarca, shows a very clear bimodal distribution of ancestries. Not only this, but this bimodal distribution has persisted for 25 generations (see Figure 1). Simulations demonstrated that gene flow is low between the subgroups at Aguazarca, on the order  < 3 Nm.

Figure 1: Distribution of ancestry in the three swordtail hybrid populations. From Schumer et al., 2017.

These results suggest that strong assortative mating is present between hybrid subgroups in Aguazarca but not in the other hybrid populations. The other populations include plenty of F1 offspring, again arguing that hybridization is common. Genotyping mother-offspring pairs further supports this finding. Aguazarca mother-offspring pairs identified no instances of hybridization, while Totonicapa showed numerous (Figure 2).

Figure 2: Observed matings in females support assortative mating in Aguazarca but not Totonicapa .

This paper is filled with interesting findings. For example, in contrast to the wild, mate preference cannot be found in the lab between Aguazarca subgroups; hybridization readily occurs. There also seems to be no visual or olfactory female preference in the lab. What is most striking to me though, is that the same hybridization event in different contexts produces very different outcomes. In two cases, a hybrid swarm formed. However, for some reason in Aguazarca assortative mating resulted in distinct subgroups. This inconsistency between replicate hybrid zones is surprising. To quote the authors,

These results suggest that even strong assortative mating observed over many generations may be an incomplete barrier to gene flow between populations. Furthermore, our findings highlight the importance of understanding the context dependence of assortative mating in understanding its potential impacts on reproductive isolation.

Fisher, H.S., Wong, B.B. and Rosenthal, G.G., 2006. Alteration of the chemical environment disrupts communication in a freshwater fish. Proceedings of the Royal Society of London B: Biological Sciences273(1591), pp.1187-1193.
Rosenthal, Gil G., Xochitl F. de la Rosa Reyna, Steven Kazianis, Matthew J. Stephens, Donald C. Morizot, Michael J. Ryan, and Francisco J. García de León. “Dissolution of sexual signal complexes in a hybrid zone between the swordtails Xiphophorus birchmanni and Xiphophorus malinche (Poeciliidae).” Copeia2003, no. 2 (2003): 299-307.
Schumer, M., Powell, D.L., Delclós, P.J., Squire, M., Cui, R., Andolfatto, P. and Rosenthal, G.G., 2017. Assortative mating and persistent reproductive isolation in hybrids. Proceedings of the National Academy of Sciences, p.201711238.

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