Reconciling concepts, theory, and empirical patterns surrounding cascade reinforcement

Reinforcement is a critically important process in speciation. It has been credited with often completing speciation, and it is unique in that natural selection directly favors the evolution of reproductive isolating barriers. Reinforcement occurs when selection favors increased prezygotic isolation between two lineages in order to avoid maladaptive hybridization in areas of sympatry (Noor 1999; Servedio and Noor 2003; Coyne and Orr 2004). The classic signature of reinforcement is reproductive character displacement (RCD), where prezygotic isolation is heightened between two lineages in areas of sympatry relative to areas of allopatry. Reinforcement was once considered controversial primarily due to theoretical difficulties (Felsenstein 1981; Spencer et al. 1986; reviewed in Noor 1999, and Coyne and Orr, 2004). However, a wealth of empirical cases demonstrating reinforcement along with renewed theoretical treatments of the process of reinforcement (Liou and Price 1994; Kelly and Noor 1996; Servedio 2000; Kirkpatrick and Ravigne 2002) has led to the conclusion that reinforcement can and does occur in nature. One consequence of reinforcement is that—by altering reproductive isolating traits—reinforcement may also lead to prezygotic isolation among populations within species. Hence, like ecological and sexual selection, reinforcement can have incidental effects upon reproductive isolation (RI). In fact, reinforcement might be particularly likely to have such incidental effects precisely because it alters reproductive isolating traits among species in areas of sympatry. The process whereby increased prezygotic isolation among populations evolves as an incidental effect of reinforcement has been referred to as “cascade reinforcement” (Ortiz-Barrientos et al. 2009) and as “reproductive character displacement speciation” (Hoskin and Higgie 2010). In this special column, we use the term cascade reinforcement. The idea has been recognized sporadically throughout the history of reinforcement (Zouros and Dentremont 1980; Howard 1993), but has recently received renewed attention (OrtizBarrientos et al. 2009; Hoskin and Higgie 2010; Abbott et al. 2013). A substantial number of empirical studies have shown patterns in prezygotic isolation among populations that are consistent with cascade reinforcement (Nosil et al. 2003; Hoskin et al. 2005; Higgie and Blows 2007, Higgie and Blows 2008; Lemmon 2009; Bewick and Dyer 2014; Pfennig and Rice 2014; Kozak et al. 2015). Two broad classes of cascade reinforcement have been recognized in the literature (Abbott et al. 2013; Comeault and Matute 2016). In this issue, Comeault and Matute (2016) refer to these as “sympatry– allopatry” effects and “convergent-sympatry” effects. To conceptualize these two types of cascade reinforcement, consider Figure 1, which shows a phylogeny with two species (A and B) and two populations within species B (B1 and B2). As noted by Pfennig (2016) in this column, the terminology surrounding these concepts can be confusing. With sympatry–allopatry effects, B1 is sympatric and B2 is allopatric with respect to A, but the two are parapatric to one another. Reinforcement between A and B1 creates preferences and traits that confer RI between them. While the isolating traits in B1 are favored in areas of sympatry with A, they are disfavored in the allopatric population, B2. A number of empirical papers are consistent with this scenario (Bewick and Dyer 2014; Pfennig and Rice 2014; Rundle and Dyer 2015). With convergent-sympatry effects, both B1 and B2 are sympatric with A but are potentially allopatric with one another. Convergent-sympatry effects occur when separate populations within a species experience reinforcement independently and convergent evolution occurs. Reinforcement is convergent in the sense that RI evolves independently between A and both B1 and B2. Reinforcement occurs in both populations but different isolating traits evolve in each, both of which create isolation from A. Because conspecific preference in populations B1 and B2 rely on different isolating traits, prezygotic isolation arises between them and can prevent gene flow upon secondary contact. Empirical work also supports this scenario (Lemmon 2009). The empirical evidence for cascade reinforcement has preceded the theoretical treatment of the phenomenon, a situation reminiscent of the earlier situation with general reinforcement. Cascade reinforcement has, until now, relied primarily on verbal models (Ortiz-Barrientos et al. 2009; Hoskin and Higgie 2010). However, two studies are noteworthy. McPeek and Gavrilets (2006) created a model that showed that interactions with other species could rapidly create impressive variation among populations within a species in female preference functions, which they assumed to be vital for the early stages of speciation. One could consider this as an early model of convergent-sympatry effects. However, this study assumed that speciation was completed with the interacting species (i.e., hybrid fitness was zero) and did not allow