A Test of Alternative Hypotheses for the Evolution of Reproductive Isolation Between Spadefoot Toads: Support for the Reinforcement Hypothesis

Abstract

Abstract. How do species that interbreed become reproductively isolated? If hybrids are less fit than parental types, natural selection should promote reproductive isolation by favoring the evolution of premating mechanisms that prevent hybridization (a process termed reinforcement). Although reinforcement should generate a decline in hybridization over time, countervailing forces of gene flow and recombination are thought to preclude natural selection from enhancing and finalizing reproductive isolation. Here, I present recent estimates of hybridization frequency between two species of spadefoot toad, Spea multiplicata and S. bombifrons. I compare these recent measures of hybrid frequency with previously published estimates and show that hybridization between these species has declined precipitously over the past 27 years. Although previous studies suggest that reinforcement possibly accounts for this decline in hybrids over time, three alternative hypotheses also can explain the observed decrease in hybridization. First, if one of the two interacting species becomes rare, opportunities for and incidence of hybridization may decrease. Second, if one of the two interacting species is initially rare, hybridization may be initially common if the rare species has difficulty locating conspecific mates. Third, if hybrids are produced only in particular environments, hybrid frequency may decline if habitat changes result in loss of those environments that promote hybrid formation. I found no support for these three alternative explanations of the decline in hybrids. Instead, reinforcement appears to best account for the evolution of enhanced reproductive isolation between these species. Moreover, the finding that hybridization declined precipitously in only 27 years suggests that many systems that have undergone reinforcement may be overlooked because reproductive isolation between the interacting populations or species may already be complete. The evolution of reproductive isolation between potentially interbreeding species or recently diverged populations is a necessary component of both the speciation process and the maintenance of species barriers. Without reproductive isolation, interbreeding would tend to break down evolved differences between species or recently diverged populations. Evaluating how reproductive isolating mechanisms evolve is therefore critical to understanding how new species form and how barriers between species are maintained.One mechanism by which reproductive isolating barriers may evolve is via natural selection. If hybrids are unfit relative to pure-species types, natural selection should favor the evolution of premating isolating mechanisms-usually mating behaviors-that prevent the production of unfit hybrids (e.g., Coyne and Orr 1989;Howard 1993;Noor 1995;Saetre et al. 1997). This process, termed reinforcement, should result in a decline of hybridization over time if the evolution of premating isolating barriers effectively enhances reproductive isolation between the two interbreeding p...

Geographic variation in hybridization across a reinforcement contact zone of chorus frogs (Pseudacris)

“…Instead the youngest contacts (Lemmon & Lemmon, 2008) had moderate (Virginia R8‐R9) levels of hybridization, whereas older contacts varied from high (Florida R2) to low (South Carolina R6 and Georgia R5; Tables 2 and 3; Figure 2). These data suggest: (1) relative timing of contact alone is not sufficient to explain variation in hybridization frequencies in sympatric regions, and (2) in accord with other studies (e.g., Matute, 2010; Pfennig, 2003), RCD can evolve rapidly relative to the decay of the phylogeographic footprint following range expansion. Thus, the current hybridization rates across populations likely either reflect equilibrium levels after contact rather than a spectrum of rates from early to established contact zones or else other factors have influenced hybridization frequencies across populations (Borge et al., 2005).…”

“…These estimates are also outside the range of frequencies estimated in another well‐studied frog reinforcement contact zone (i.e., 0.3%–6% F1 hybrids; Pfennig & Simovich, 2002; Pfennig, 2003). One question is whether these estimates reflect historical or present‐day hybridization, or more specifically, was there a high rate of hybridization upon initial secondary contact followed by a decline in rate through time?…”

“…2001; Dobzhansky, 1940; Jones, 1973). Longitudinal studies of reinforcement contact zones through time are consistent with this prediction (Pfennig, 2003; Pfennig & Simovich, 2002). An additional approach for testing this prediction is to compare levels of hybridization in older versus more recent contact zones.…”

“…This prediction was derived from the expectation that hybridization rates should decline through time as reinforcement proceeds (Blair, 1974; Britch, Cain, M. L., & Howard, D. J. 2001; Coyne & Orr, 2004; Dobzhansky, 1940; Jones, 1973; Nosil, 2012; Pfennig, 2003). Instead the youngest contacts (Lemmon & Lemmon, 2008) had moderate (Virginia R8‐R9) levels of hybridization, whereas older contacts varied from high (Florida R2) to low (South Carolina R6 and Georgia R5; Tables 2 and 3; Figure 2).…”

Mating with the wrong species can be right

“…Her suggestion arises from a mate choice experiment with two American spadefoot toad species, Spea bombifrons (BB) and Spea multiplicana (MM). The experiment was motivated by previous field and lab studies by the author and her co-workers [14,15]. The major results from these studies are summarized in Table 1.…”