Asymmetry in reproductive isolation and its effect on directional mitochondrial introgression in the parapatric ground beetles <i>Carabus yamato</i> and <i>C. albrechti</i>

<jats:title>Abstract</jats:title><jats:p>Speciation studies seek to clarify the origin of reproductive isolation, the various mechanisms working from mate recognition through postzygotic stages. Asymmetric effects of isolating barriers can result in asymmetrical gene introgression during interspecific hybridization. The flightless ground beetles <jats:italic>Carabus yamato</jats:italic> and <jats:italic>C. albrechti</jats:italic> are distributed parapatrically in Japan, showing repeated asymmetrical introgression of mitochondria from <jats:italic>C. albrechti</jats:italic> to <jats:italic>C. yamato</jats:italic>. This pattern suggests that reproductive isolation between these species is strong, but incomplete and asymmetric (i.e., weaker for the cross between a <jats:italic>C. albrechti</jats:italic> female and a <jats:italic>C. yamato</jats:italic> male). To test this hypothesis, we conducted interspecific mating experiments in the laboratory. The estimates of total reproductive isolation, which occurred mainly at the premating and postmating/prezygotic stages, were high (isolation index = 0.964 for <jats:italic>C. yamato</jats:italic> female × <jats:italic>C. albrechti</jats:italic> male and 0.886 for the reciprocal cross), supporting the hypothesis of strong, but incomplete isolation. However, the observed difference between the reciprocal crosses was not sufficiently large to conclude that it caused directional introgression of mitochondria. Instead, we found asymmetry in individual isolating barriers in the postmating/prezygotic stages that coincided with the prediction, perhaps resulting from morphological mismatch of heterospecific genitalia. Although this asymmetry was compensated for by an inverse asymmetry of isolation in the postzygotic stage, the contribution of these individual barriers to total isolation may change for our expectation when considering females mating with multiple heterospecific males.</jats:p>