Both morph‐ and species‐dependent asymmetries affect reproductive barriers between heterostylous species

Abstract

The interaction between floral traits and reproductive isolation is crucial to explaining the extraordinary diversity of angiosperms. Heterostyly, a complex floral polymorphism that optimizes outcrossing, evolved repeatedly and has been shown to accelerate diversification in primroses, yet its potential influence on isolating mechanisms remains unexplored. Furthermore, the relative contribution of pre‐ versus postmating barriers to reproductive isolation is still debated. No experimental study has yet evaluated the possible effects of heterostyly on pre‐ and postmating reproductive mechanisms. We quantify multiple reproductive barriers between the heterostylous Primula elatior (oxlip) and P. vulgaris (primrose), which readily hybridize when co‐occurring, and test whether traits of heterostyly contribute to reproductive barriers in unique ways. We find that premating isolation is key for both species, while postmating isolation is considerable only for P. vulgaris; ecogeographic isolation is crucial for both species, while phenological, seed developmental, and hybrid sterility barriers are also important in P. vulgaris, implicating sympatrically higher gene flow into P. elatior. We document for the first time that, in addition to the aforementioned species‐dependent asymmetries, morph‐dependent asymmetries affect reproductive barriers between heterostylous species. Indeed, the interspecific decrease of reciprocity between high sexual organs of complementary floral morphs limits interspecific pollen transfer from anthers of short‐styled flowers to stigmas of long‐styled flowers, while higher reciprocity between low sexual organs favors introgression over isolation from anthers of long‐styled flowers to stigmas of short‐styled flowers. Finally, intramorph incompatibility persists across species boundaries, but is weakened in long‐styled flowers of P. elatior, opening a possible backdoor to gene flow through intramorph pollen transfer between species. Therefore, patterns of gene flow across species boundaries are likely affected by floral morph composition of adjacent populations. To summarize, our study highlights the general importance of premating isolation and newly illustrates that both morph‐ and species‐dependent asymmetries shape boundaries between heterostylous species.

Is sexual organ reciprocity related to legitimate pollen deposition in distylous Pulmonaria (Boraginaceae)?

“…2), pollinators may not be able to distinguish between flowers of different Pulmonaria species in sympatric populations, which creates opportunities for interspecific gene flow and hybridization. Keller et al (2012Keller et al ( , 2016 investigated whether differences in reciprocity affected possibilities for gene flow among three distylous Primula species. Their results showed that interspecific decrease of reciprocity between high sexual organs of complementary floral morphs limited interspecific pollen transfer from anthers of shortstyled flowers to stigmas of long-styled flowers.…”

Mixed Mating in Homostylous Species: Genetic and Experimental Evidence from an Alpine Plant with Variable Herkogamy,Primula halleri

“…However, several studies found herkogamy to have a strong genetic basis (e.g., Herlihy and Eckert 2007;Luo and Widmer 2013), and a comprehensive review concluded that the trait is typically highly heritable and evolvable (Opedal et al 2017). Moreover, the profound functional implications of sexual organ position Keller et al 2012Keller et al , 2014Keller et al , 2016) justify speculating about possible adaptive explanations for the existence of high-herkogamous plants.…”

Recurrent hybridisation events between Primula vulgaris, P. veris and P. elatior (Primulaceae, Ericales) challenge the species boundaries: using molecular markers to re‐evaluate morphological identifications

“…He found low pollen fertility, which is common in hybrids, in many of what appeared to be pure species, indicating that the individuals were in fact backcrossed hybrids. Keller et al (2016) found that the reproductive barriers upholding species integrity were weakened in the hybrids, allowing for introgression, especially in P. elatior. This is in accordance with our findings; that even though the three sympatric species on Møn appear pure, many of the investigated markers pointed to backcrossing and introgression.…”

“…The difference in inflorescence morphology may play a role, since the solitary flower raised on a pedicel allows P. vulgaris to develop and open its flowers relatively quickly in its open, sun-exposed, warm localities, where P. vulgaris occupies a different niche than P. elatior, which is found in shadier locations. Keller et al (2016) modelled the reproductive barriers between P. vulgaris and P. elatior in a series of experiments to evaluate pre-and postmating barriers and the significance of the heteromorphic flowers. They found that the types of floral morphs involved in the crosses also played a part in fertility.…”