The importance of autonomous selfing in preventing hybridization in three closely related plant species

Abstract

Summary In plants that are able to self‐fertilize, autonomous selfing has been hypothesized to function as an effective mechanism that prevents heterospecific mating. However, there have only been few studies that have assessed the relative and absolute contribution of different modes of selfing to total reproductive isolation acting between species. Because selfing can be expected to increase fitness costs when offspring are sired from more outcrossing sister taxa, it can be hypothesized that the contribution of post‐zygotic barriers to total reproductive isolation becomes stronger in selfing than in more outcrossing relatives. To assess the efficiency of different modes of selfing against heterospecific mating, we conducted mixed‐pollination experiments in three Centaurium species showing strong differences in mating system (i.e. delayed selfing in Centaurium erythraea, competing selfing in C. littorale and prior selfing in C. pulchellum). The contribution of selfing to total reproductive isolation was further examined by quantifying the strength of three pre‐zygotic (flowering phenology, pollinator fidelity and pollen production) and four intrinsic post‐zygotic (seed set and germination, survival and flowering capacity) barriers for each of the six species pair combinations. Although autonomous selfing as a reproductive barrier was unable to completely impede gene flow, its efficiency as a mechanism to prevents heterospecific pollination strongly depended on the mode of selfing, with prior selfing being by far the most efficient mechanism and delayed selfing only offering a limited protection against hybrid fertilization at the end of a flower's lifetime. Apart from the prevention effect of selfing, differences in pollinator fidelity and pollen production also contributed substantially to total reproductive isolation. Post‐zygotic hybrid costs were high and most prevalent for seed production and germination success. Reductions in hybrid vigour were significantly associated with the mating system of the maternal species, with the highest reductions in the most selfing C. pulchellum and the lowest reductions in predominant outcrossing C. erythraea. Synthesis. Our findings indicate that selfing may prevent species from interspecific gene flow and hybridization. The association between the capacity to self‐autonomously and hybrid vigour further suggests that selfing may foster post‐zygotic costs following hybridization.

Shifts to earlier selfing in sympatry may reduce costs of pollinator sharing

“…Brys et al. () similarly found that timing of selfing among Centaurium species was critical to determining the risk of hybridization, with prior selfing clearly serving as the most efficient barrier to hybridization. Our study is unique in demonstrating a general pattern of divergence between allopatric and sympatric populations within a species in the timing of selfing, providing the first evidence for this fundamental signature of reproductive character displacement due to reinforcement (reviewed in Brown and Wilson ; Schluter and McPhail ; Servedio and Noor ).…”

“…In this way, autonomous selfing that occurs before opportunities for HPT could be considered a preemptive action that protects against fitness losses through gamete loss to and hybridization with congeners, a hypothesis recently outlined by Brys et al. () that we term the “preemptive selfing hypothesis.”…”

“…In contrast, delayed selfing would not serve as an effective barrier to the risks of pollinator movement between coflowering congeners. Under conditions where pollinator movement between species are common, delayed selfing would fail to block heterospecific pollen receipt or pollen export to heterospecifics, and therefore would fail to prevent gamete (pollen and ovule) loss or to alter hybridization rates between congeners (Brys et al 2016). Competing autonomous selfing could alleviate the risks of heterospecific pollen receipt where there is conspecific pollen precedence or where heterospecific pollen effects depend on the ratio of conspecific to heterospecific pollen deposited.…”

Immigrant and extrinsic hybrid seed inviability contribute to reproductive isolation between forest and dune ecotypes of Epipactis helleborine (Orchidaceae)

“…Because several studies have shown that Epipactis species can rapidly evolve towards selfing (Pedersen and Ehlers , Squirrell et al , Brys and Jacquemyn ) and because selfing itself can act as a reproductive barrier preventing interspecific mating (Brys et al ), we investigated whether the capacity to self autonomously differed between the two ecotypes. Two months before flowering, ten individuals were selected in one forest and one dune population and transferred to a pollinator‐free greenhouse.…”

The best of both worlds? A review of delayed selfing in flowering plants

“…Finally, early selfing might be selected for if it reduces interspecific pollen transfer. In contrast to delayed selfing, earlier selfing can reduce loss of fitness through production of hybrid offspring and would be favored under conditions in which hybridization invokes a high fitness cost (Goodwillie and Ness, 2013;Brys et al, 2016).…”