Sibling Competition Arena: Selfing and a Competition Arena Can Combine to Constitute a Barrier to Gene Flow in Sympatry

Abstract

Closely related species coexisting in sympatry provide critical insight into the mechanisms underlying speciation and the maintenance of genetic divergence. Selfing may promote reproductive isolation by facilitating local adaptation, causing reduced hybrid fitness in parental environments. Here, we propose a novel mechanism by which selfing can further impair interspecific gene flow: selfing may act to ensure that nonhybrid progeny systematically co-occur whenever hybrid genotypes are produced. Under a competition arena, the fitness differentials between nonhybrid and hybrid progeny are then magnified, preventing development of interspecific hybrids. We investigate whether this "sibling competition arena" can explain the coexistence in sympatry of closely related species of the plant fungal pathogens (Microbotryum) causing anther-smut disease. The probabilities of intrapromycelial mating (automixis), outcrossing, and sibling competition were manipulated in artificial inoculations to evaluate their contribution to reproductive isolation. We report that both intrapromycelial selfing and sibling competition significantly reduced rates of hybrid infection beyond that expected based solely upon selfing rates and noncompetitive fitness differentials between hybrid and nonhybrid progeny. Our results thus suggest that selfing and a sibling competition arena can combine to constitute a barrier to gene flow and diminish selection for additional barriers to gene flow in sympatry. K E Y W O R D S :Assortative mating, fungi, hybridization, prezygotic isolating mechanism, postzygotic reproductive isolation, selection arena, Silene, speciation.

The tempo and modes of evolution of reproductive isolation in fungi

“…The explanation for the persistence of high degree of syngamy compatibility at large genetic distance may instead be that the strength of selection for increasing assortative mating via mate choice may be too low in Microbotryum, because hybridization is sufficiently rare in nature. The cumulative effects of other presyngamy barriers, such as differences in habitat and pollinator of the plant Evolution of reproductive isolation in fungi T Giraud and S Gourbière species (Goulson and Jerrim, 1997;van Putten et al, 2007;Gladieux et al, 2010b) and high rates of selfing (40.90;Giraud et al, 2005Giraud et al, , 2008bHood and Antonovics, 2000;Gladieux et al, 2010b), may be strong enough such that very few hybrids are produced in nature even with weak preference for conspecifics (Bucheli et al, 2000;Refrégier et al, 2010;Gladieux et al, 2010b;Gibson et al, 2012).…”

Experimental hybridization and backcrossing reveal forces of reproductive isolation in Microbotryum

“…Generally, most Microbotryum species have high selfing rates [24], thus limiting the probability of interspecific gene flow [26-28]. Mechanisms of pre-mating barriers in the form of assortative mating have been investigated but not found [29,30].…”

Performance of a Hybrid Fungal Pathogen on Pure-Species and Hybrid Host Plants

“…Inoculum preparation was conducted as described in Gibson et al (2012). Briefly, for each Microbotryum sample, a single anther was extracted from preserved diseased flowers and serially diluted prior to growth on GMB2 medium (Thomas et al 2003).…”

“…However, very few S. dioica plants successfully flowered under greenhouse conditions, so this host was excluded from the following analyses. Seed sterilization and germination in preparation for inoculation were conducted as described in Gibson et al (2012).…”