Sperm divergence in a passerine contact zone: Indication of reinforcement at the gametic level

Abstract

Postcopulatory sexual selection may promote evolutionary diversification in sperm form, but the contribution of between‐species divergence in sperm morphology to the origin of reproductive isolation and speciation remains little understood. To assess the possible role of sperm diversification in reproductive isolation, we studied sperm morphology in two closely related bird species, the common nightingale (Luscinia megarhynchos) and the thrush nightingale (Luscinia luscinia), that hybridize in a secondary contact zone spanning Central and Eastern Europe. We found: (1) striking divergence between the species in total sperm length, accompanied by a difference in the length of the mitochondrial sperm component; (2) greater divergence between species in sperm morphology in sympatry than in allopatry, with evidence for character displacement in sperm head length detected in L. megarhynchos; (3) interspecific hybrids showing sperm with a length intermediate between the parental species, but no evidence for decreased sperm quality (the proportion of abnormal spermatozoa in ejaculates). Our results demonstrate that divergence in sperm morphology between the two nightingale species does not result in intrinsic postzygotic isolation, but may contribute to postcopulatory prezygotic isolation. This isolation could be strengthened in sympatry by reinforcement.

Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances

“…For example, Matute (2010) detected an increase in PMPZ barriers between sympatric D. yakuba and D. santomea, where D. yakuba females depleted the sperm of D. santomea males faster than that of conspecific males. Also, sympatric populations of two nightingale species (Luscinia) showed greater divergence in sperm morphology than the allopatric ones, with evidence for character displacement in sperm head length in one species (Albrecht et al 2019). In our study, species differences in the length of female seminal receptacle (D. montana: 3.43 mm; D. flavomontana: 10.54 mm) and male sperm (D. montana: 3.34 mm;D.…”

“…Also, sympatric populations of two nightingale species ( Luscinia ) showed greater divergence in sperm morphology than the allopatric ones, with evidence for character displacement in sperm head length in one species (Albrecht et al. ). In our study, species differences in the length of female seminal receptacle ( D. montana : 3.43 mm; D. flavomontana : 10.54 mm) and male sperm ( D. montana : 3.34 mm; D. flavomontana : 5.53 mm; Pitnick et al.…”

“…PMPZ barriers, including incompatibilities in the transfer, storage, and use of heterospecific sperm, involve discordant interactions between heterospecific gametes and/or between the female reproductive tract and male seminal fluids (Howard 1999;Wirtz 1999;Price et al 2001;Howard et al 2009). Reinforcement of these barriers has been reported so far only between Drosophila yakuba and Drosophila santomea (Matute 2010) and Drosophila pseudoobscura and Drosophila persimilis (Castillo and Moyle 2017) and between two nightingale species (Luscinia megarhynchos and Luscinia luscinia; Albrecht et al 2019). Notably, strong PMPZ barriers can act as a driving force in the reinforcement of premating barriers, and selection pressure generated by them can be as strong or even stronger than that caused by low hybrid fitness (Servedio 2001).…”

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

“…Reinhold, & Engqvist, 2016). However, reinforcing selection is also predicted to favour the evolution of enhanced PMPZ barriers (Lorch & Servedio, 2007) and has been reported in at least four cases (Albrecht et al, 2019;Castillo & Moyle, 2019;Matute, 2010;Poikela et al, 2019). To our knowledge, only one study has compared patterns of CSP between allopatric and sympatric populations (Castillo & Moyle, 2019), and they found patterns of CSP consistent with reinforcement.…”

“…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., ). To our knowledge, only one study has compared patterns of CSP between allopatric and sympatric populations (Castillo & Moyle, ), and they found patterns of CSP consistent with reinforcement.…”