Females discriminate against heterospecific sperm in a natural hybrid zone

Abstract

When hybridization is maladaptive, species-specific mate preferences are selectively favored, but low mate availability may constrain species-assortative pairing. Females paired to heterospecifics may then benefit by copulating with multiple males and subsequently favoring sperm of conspecifics. Whether such mechanisms for biasing paternity toward conspecifics act as important reproductive barriers in socially monogamous vertebrate species remains to be determined. We use a combination of long-term breeding records from a natural hybrid zone between collared and pied flycatchers (Ficedula albicollis and F. hypoleuca), and an in vitro experiment comparing conspecific and heterospecific sperm performance in female reproductive tract fluid, to evaluate the potential significance of female cryptic choice. We show that the females most at risk of hybridizing (pied flycatchers) frequently copulate with multiple males and are able to inhibit heterospecific sperm performance. The negative effect on heterospecific sperm performance was strongest in pied flycatcher females that were most likely to have been previously exposed to collared flycatcher sperm. We thus demonstrate that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate. While the evolutionary history of this barrier is unknown, our results imply that there is opportunity for it to be accentuated via a reinforcement-like process.

Possible glimpses into early speciation: the effect of ovarian fluid on sperm velocity accords with post‐copulatory isolation between two guppy populations

“…testing more than two populations, from a range of geographical origins). However, our results are in line with previous studies that evaluated the presence of similar reproductive barriers acting among (Yeates et al ., ; Cramer et al ., ) and within species (Beirao et al ., ). Nevertheless, our findings indicate some complexity in the observed patterns at the within‐species level, where the direction of the effect depended on the specific combination of populations examined.…”

“…Indeed, sperm–ovarian fluid interactions represent a post‐mating inbreeding avoidance mechanism in guppies, as sperm swimming speed – and ultimately competitive fertilization success – is reduced when sperm are exposed to ovarian fluid from a sister compared to an unrelated female (Gasparini & Pilastro, ). Recent studies highlight the importance of ovarian fluid in generating reproductive barriers across different species (Yeates et al ., ; Cramer et al ., ). Here, we test the novel hypothesis that ovarian fluid will also mediate initial reproductive barriers at the population level by differentially affecting sperm swimming performance.…”

“…conspecific sperm precedence, e.g. Birkhead & Brillard, ; Howard et al ., ; Manier et al ., ; Shaw & Lambert, ; Cramer et al ., ,b).…”

Divergence in style length and pollen size leads to a postmating‐prezygotic reproductive barrier among populations of Silene latifolia

“…Asymmetry in reproductive isolating barriers is pervasive across taxa for both animals (Martin-Coello et al 2009;Schrader et al 2013;Manier et al 2013;Cramer et al 2016) and plants (Sorensson et al 1994;Tiffin et al 2001;Turelli and Moyle 2001), and is especially common in the early stages of reproductive isolation (Runquist et al 2013). Asymmetry in reproductive isolating barriers is pervasive across taxa for both animals (Martin-Coello et al 2009;Schrader et al 2013;Manier et al 2013;Cramer et al 2016) and plants (Sorensson et al 1994;Tiffin et al 2001;Turelli and Moyle 2001), and is especially common in the early stages of reproductive isolation (Runquist et al 2013).…”

“…Conspecific sperm precedence has been shown to severely limit the production of interspecific hybrids in crosses between species (e.g., Howard et al 1998;Chang 2004), sometimes in an asymmetric way (Cramer et al 2016). Conspecific sperm precedence has been shown to severely limit the production of interspecific hybrids in crosses between species (e.g., Howard et al 1998;Chang 2004), sometimes in an asymmetric way (Cramer et al 2016).…”