Experimental evolution reveals balancing selection underlying coexistence of alternative male reproductive phenotypes.

Heritable alternative reproductive phenotypes (ARPs), which differ in traits associated with competition for mates, occur across taxa. If polymorphism in the genes underlying ARPs is maintained by balancing selection, selection should return ARP proportions to their equilibrium if that equilibrium is perturbed. Here, we used an experimental evolution approach to directly test this prediction in male Rhizoglyphus robini, in which two heritable morphs occur: armored fighters and more female-like, benign scramblers. Using selection lines nearly fixed for male morph, we constructed replicate populations consisting of 50% or 94% fighters, and allowed them to evolve for 14 generations in two types of environment: simple or spatially complex. We found that in both types of populations, the proportion of fighters converged on values within a narrow range of 0.70-0.83, although the rate of convergence was slower in the complex environment. Our results thus demonstrate balancing selection acting on polymorphism(s) underlying ARPs.

Selection for alternative male reproductive tactics alters intralocus sexual conflict.

Intralocus sexual conflict (IASC) arises when fitness optima for a shared trait differ between the sexes; such conflict may help maintain genetic variation within populations. Sex-limited expression of sexually antagonistic traits may help resolve the conflict, but the extent of this resolution remains a subject of debate. In species with alternative male reproductive tactics, unresolved conflict should manifest more in a more sexually dimorphic male phenotype. We tested this prediction in the bulb mite (Rhizoglyphus robini), a species in which aggressive fighters coexist with benign scramblers. To do this, we established replicated lines in which we increased the proportion of each of the alternative male morphs using artificial selection. After approximately 40 generations, the proportion of fighters and scramblers stabilized at >0.9 in fighter- and scrambler-selected lines, respectively. We then measured several female fitness components. As predicted by IASC theory, female fecundity and longevity were lower in lines selected for fighters and higher in lines selected for scramblers. This finding indicates that sexually selected phenotypes are associated with an ontogenetic conflict that is not easily resolved. Furthermore, we suggest that IASC may be an important mechanism contributing to the maintenance of genetic variation in the expression of alternative reproductive tactics.

No evidence for reproductive isolation through sexual conflict in the bulb mite Rhizoglyphus robini.

Sexual conflict leading to sexual antagonistic coevolution has been hypothesized to drive reproductive isolation in allopatric populations and hence lead to speciation. However, the generality of this speciation mechanism is under debate. We used experimental evolution in the bulb mite Rhizoglyphusrobini to investigate whether sexual conflict promotes reproductive isolation measured comprehensively to include all possible pre- and post-zygotic mechanisms. We established replicate populations in which we either enforced monogamy, and hence removed sexual conflict by making male and female evolutionary interests congruent, or allowed promiscuity. After 35 and 45 generations of experimental evolution, we found no evidence of reproductive isolation between the populations in any of the mating systems. Our results indicate that sexual conflict does not necessarily drive fast reproductive isolation and it may not be a ubiquitous mechanism leading to speciation.

Mating system affects population performance and extinction risk under environmental challenge.

Failure of organisms to adapt to sudden environmental changes may lead to extinction. The type of mating system, by affecting fertility and the strength of sexual selection, may have a major impact on a population's chances to adapt and survive. Here, we use experimental evolution in bulb mites (Rhizoglyphus robini) to examine the effects of the mating system on population performance under environmental change. We demonstrate that populations in which monogamy was enforced suffered a dramatic fitness decline when evolving at an increased temperature, whereas the negative effects of change in a thermal environment were alleviated in polygamous populations. Strikingly, within 17 generations, all monogamous populations experiencing higher temperature went extinct, whereas all polygamous populations survived. Our results show that the mating system may have dramatic effects on the risk of extinction under environmental change.