Cryptic gametic interactions confer both conspecific and heterospecific advantages in the Chrysochus (Coleoptera: Chrysomelidae) hybrid zone

Abstract

Most species pairs are isolated through the collective action of a suite of barriers. Recent work has shown that cryptic barriers such as conspecific sperm precedence can be quite strong, suggesting that they evolve quickly. However, because the strength of multiple barriers has been formally quantified in very few systems, the relative speed with which conspecific sperm precedence evolves remains unclear. Here, we measure the strength of both conspecific sperm precedence and cryptic non-competitive isolation between the hybridizing sister species, Chrysochus auratus and C. cobaltinus (Coleoptera: Chrysomelidae), and compare the strength of those barriers to the strength of other known reproductive barriers in this system. Overall, cryptic barriers in this system are weaker than other barriers, indicating that they have not evolved rapidly. Furthermore, their evolution has been asymmetric. Non-competitive barriers substantially reduce the production of hybrid offspring by C. auratus females but not by C. cobaltinus females. In multiply-mated C. cobaltinus females, heterospecific sperm outcompete conspecific sperm, as evidenced by the fact that heterospecific males sired disproportionately more offspring than predicted from the results for singly-mated females. In C. auratus females, neither sperm type has a competitive advantage. Such asymmetries explain why nearly all F1 hybrids in the field are from crosses between C. cobaltinus females and C. auratus males. We discuss these findings in terms of understanding the cost of mating 'mistakes' in the Chrysochus hybrid zone. In addition, our discovery that 95% confidence intervals for commonly-used isolation statistics can be very wide has important implications for speciation research. Specifically, to avoid biases in the interpretation of such isolation metrics, we suggest that studies should routinely include error estimates in their analyses of reproductive isolation.

The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers

“…Heterospecific mating frequency and multiple mating had very different impacts on two species of hybridizing Chrysochus beetles. Auratus females maintained a low level of F1 production across heterospecific mating frequencies up to 70% (Figure ), consistent with previous evidence that these females benefit from CSP in addition to noncompetitive barriers (Peterson et al., ). At all but the most extreme heterospecific mating frequencies, auratus females that mated with both species had the same number of conspecific offspring as auratus females mated to a single conspecific male.…”

“…Therefore, there is no evidence that auratus females receive fitness benefits from multiple heterospecific matings via a combination of strong CSP and enhanced fecundity. Cobaltinus females produced F1 hybrid offspring nearly proportional to their heterospecific mating frequency, supporting previous findings of a noncompetitive barriers and a lack of CSP in these females (Peterson et al., ). In fact, cobaltinus females may experience heterospecific sperm precedence, given that cobaltinus females mated to heterospecific males have fewer conspecific offspring than expected based on single matings (Peterson et al., ) and in comparison with multiple conspecific matings (e.g.…”

“…“rarer‐female effect”), whereas cobaltinus females should evolve enhanced prezygotic barriers at all relative abundances (Hoskin, Higgie, McDonald, & Moritz, ; Noor, ; Nosil et al., ; Poikela et al., ; Yukilevich, ). It may be that Chrysochus females are limited in their ability to evolve premating barriers—mate choice appears to be largely driven by males, and females cannot avoid most mating attempts (Peterson et al., ; see also Soudi, Reinhold, & Engqvist, ). However, reinforcing selection is also predicted to favour the evolution of enhanced PMPZ barriers (Lorch & Servedio, ) and has been reported in at least four cases (Albrecht et al., ; Castillo & Moyle, ; Matute, ; Poikela et al., ).…”

“…After a female completed her assigned matings, we collected her egg masses every 1‐2 days for the remainder of her lifespan. We placed egg masses in individual 0.5‐μl tubes (one mass/tube) and incubated them in the same conditions as the adults (see Peterson et al., ). After an initial 18‐day incubation (the minimum time required for hatching), we checked egg masses for hatched larvae every 1–2 days.…”

Noncompetitive Gametic Isolation between Sibling Species of Cricket: A Hypothesized Link between Within-Population Incompatibility and Reproductive Isolation between Species

“…Examples of this phenotype acting as a mechanism to reproductively isolate species can be found across the phylogeny of insects (e.g., green lacewings [13, 14], crickets [8, 15], walking sticks [16], beetles [17–19], wasps [20], and flies [21–23]). Therefore, our understanding of this phenotype in Allonemobius could shed light on a common mechanism of reproductive isolation in insects.…”