Reinforcement generates reproductive isolation between neighbouring conspecific populations of spadefoot toads

Abstract

Reproductive character displacement is the adaptive evolution of traits that minimize deleterious reproductive interactions between species. When arising from selection to avoid hybridization, this process is referred to as reinforcement. Reproductive character displacement generates divergence not only between interacting species, but also between conspecific populations that are sympatric with heterospecifics versus those that are allopatric. Consequently, such conspecific populations can become reproductively isolated. We compared female mate preferences in, and evaluated gene flow between, neighbouring populations of spadefoot toads that did and did not occur with heterospecifics (mixed-and pure-species populations, respectively). We found that in mixed-species populations females significantly preferred conspecifics. Such females also tended to prefer a conspecific call character that was dissimilar from heterospecifics. By contrast, females from pure-species populations did not discriminate conspecific from heterospecific calls. They also preferred a more exaggerated conspecific call character that resembles heterospecific males. Moreover, gene flow was significantly reduced between mixed-and pure-species population types. Thus, character displacement (and, more specifically, reinforcement) may initiate reproductive isolation between conspecific populations that differ in interactions with heterospecifics.

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement inDrosophila yakuba

“…Reinforcement in D. yakuba, therefore, adds to the growing number of examples demonstrating that locally adaptive phenotypes subject to reinforcing selection can have costs outside of regions of sympatry [18][19][20][21][22][23][24]. These examples provide evidence that the pattern of RCD frequently described in cases of reinforcement can be actively maintained by selection acting on 'reinforced' alleles between allopatric and sympatric conspecific populations.…”

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

“…Evidence for cascade reinforcement (Hoskin & Higgie, 2010; Howard, 1993; Ortiz‐Barrientos, Grealy, A., & Nosil, P. 2009) is accumulating rapidly across a taxonomically broad set of organisms (Bewick & Dyer, 2014; Dyer et al., 2013; Higgie & Blows, 2008; Hoskin, Higgie, M., McDonald, K. R., & Moritz, C. 2005; Humphreys, Rundle, H. D., & Dyer, K. A. 2016; Kozak et al., 2015; Pfennig & Rice, 2014; Porretta & Urbanelli, 2012; Rice & Pfennig, 2010; Rice et al., 2016; Richards‐Zawacki & Cummings, 2011). Our data are consistent with the expectation that cascade reinforcement cannot only promote the rapid divergence of reproductive behaviors among different populations (Lemmon, 2009) but also drive intraspecific genetic divergence at neutral loci (Rice & Pfennig, 2010).…”

“…As a consequence reproductive behaviors may diversify across the distributions of taxa (Bewick & Dyer, 2014; Dyer, White, Sztepanacz, Bewick, & Rundle, 2013; Hoskin et al., 2005; Humphreys, Rundle, & Dyer, 2016; Kozak et al., 2015; Porretta & Urbanelli, 2012; Rice & Pfennig, 2010). Thus, we might predict that species experiencing reinforcement would also exhibit elevated levels of genetic differentiation across their geographic distributions, such as between allopatry and sympatry (Pfennig & Rice, 2014; Rice, McQuillan, Seears, & Warren, 2016). Furthermore, in cases of more complex species interactions, such as where three or more species interact across a contact zone, the divergent selection pressures may further accelerate genetic diversification across sympatric populations originating from different communities.…”

Behavioral Isolation due to Cascade Reinforcement in Lucania Killifish

“…There have been no theoretical studies of this process, and we currently rely on verbal models and empirical data (but see McPeek and Gavrilets 2006). Cascade reinforcement has been previously documented in several species of amphibians (Hoskin et al 2005;Lemmon 2009; Rice and Pfennig 2010;Richards-Zawacki and Cummings 2011;Pfennig and Rice 2014) and insects (walking sticks [Nosil et al 2003], rock-pool beetles [Porretta and Urbanelli 2012], and fruit flies [Jaenike et al 2006;Blows 2007, 2008;Dyer et al 2014]). However, the behavioral isolation that results from cascade reinforcement differs substantially across systems.…”