Evolution of Postzygotic Reproductive Isolation in a Guild of Deceptive Orchids

Abstract

The evolution of reproductive barriers is of central importance for speciation. Here, we investigated three components of postzygotic isolation-embryo mortality, hybrid inviability, and hybrid sterility-in a group of food-deceptive Mediterranean orchids from the genera Anacamptis, Neotinea, and Orchis. In these orchids, pollinator-mediated isolation is weak, which suggests that postpollination barriers exist. Based on crossing experiments and a literature survey, we found that embryo mortality caused complete reproductive isolation among 36.3% of the species pairs, and hybrid inviability affected 55.6% of the potentially hybridizing species pairs. Hybrid sterility was assessed experimentally for seven species pairs. A strong reduction of fertility in all investigated hybrids was found, together with clear differences between male and female components of hybrid sterility. Postzygotic isolation was found to evolve gradually with genetic divergence, and late postzygotic isolation (i.e., hybrid inviability and sterility) evolved faster than embryo mortality, which is an earlier postzygotic isolation stage. These results reveal that intrinsic postzygotic isolation strongly contributes to maintaining species boundaries among Mediterranean food-deceptive orchids while establishing a prominent role for these reproductive barriers in the early stage of species isolation.

Evolution of reproductive isolation in plants

“…A common pattern that was found in the studies of Moyle et al (2004) and Scopece et al (2007Scopece et al ( , 2008 is that the strength of postzygotic barriers increases with increasing genetic distance among taxa. These studies have focused on intrinsic postzygotic barriers, with the exception of Scopece et al (2008) where both intrinsic and extrinsic barriers may interact to cause the observed hybrid inviability.…”

“…In a second study on the same groups of orchids, Scopece et al (2008) found that postzygotic isolation evolved gradually with genetic divergence at each of the three investigated stages, and that late postzygotic isolation (that is, hybrid sterility and hybrid inviability) evolved faster than early postzygotic isolation (that is, embryo mortality). Of the late postzygotic isolation factors, hybrid sterility most likely evolved faster than hybrid inviability.…”

“…The observation made in animals that prezygotic barriers evolve faster than postzygotic ones has thus far not been confirmed in plants (Moyle et al, 2004;Scopece et al, 2007Scopece et al, , 2008. Whether this is a consequence of a more complex genetic architecture underlying prezygotic barriers in plants (discussed below) or is due to the fact that in contrast to animals, plants cannot directly choose their mate but depend on often unreliable pollinator service for successful gamete transfer, remains to be tested.…”

“…These studies have focused on intrinsic postzygotic barriers, with the exception of Scopece et al (2008) where both intrinsic and extrinsic barriers may interact to cause the observed hybrid inviability. However, the experimental design in Scopece et al (2008) did not allow to disentangle extrinsic and intrinsic causes of hybrid inviability.…”

Genomic collinearity and the genetic architecture of floral differences between the homoploid hybrid species Iris nelsonii and one of its progenitors, Iris hexagona

“…The evolution of new, reproductively isolated species usually involves the gradual accumulation of multiple prezygotic and postzygotic reproductive isolating barriers over time Orr, 1989, 1997;Moyle et al, 2004;Malone and Fontenot, 2008;Scopece et al, 2008). An exception to this is hybrid speciation, where reproductive isolation can evolve quite quickly (James and Abbott, 2005;Mallett, 2007;Buerkle and Rieseberg, 2008).…”