REPRODUCTIVE ISOLATION AND SPECIATION IN CLARKIA
NSF Evolutionary Processes (2018-2022)
NSF Evolutionary Processes (2010-2014)
Understanding the speciation process remains a central problem in evolutionary biology. Among the many traits hypothesized to affect speciation, those controlling “who mates with whom” stand out as having a direct link to the formation of reproductive isolation. This includes mating system, which describes the extent of self-fertilization versus outcrossing. Phylogenetic studies suggest that mating system affects speciation events and diversification rates, but the microevolutionary role of mating system in directly promoting reproductive isolation has received surprisingly little attention. Our research integrates field experiments, theory, and genomics to examine how mating system divergence generates and reinforces reproductive isolation.
The genus Clarkia (Onagraceae), with at least 12 selfer-outcrosser sister taxa, provides fertile ground for testing the role of mating system in speciation. Clarkia xantiana consists of two diploid, self-compatible annual subspecies. Outcrossing rates differ substantially between them: ssp. xantiana is primarily outcrossing and ssp. parviflora is primarily autonomously selfing.
Our previous work has shown that the two subspecies diverged very recently, ~65 kya. The selfer, parviflora forms a monophyletic group derived from xantiana (Pettengill and Moeller 2012a). Phylogeographic analyses suggest that the taxa diverged in allopatry and have subsequently expanded their ranges to a zone of secondary sympatry. Results of paleoclimatic distribution modeling reinforce this conclusion as they suggest the subspecies ranges were restricted to the southern extreme of their range and were largely non-overlapping during the last glacial maximum (Pettengill and Moeller 2012b). The narrow region of secondary sympatry includes replicated contact zones across a broad north-south geographic expanse.Left: Population phylogeny and Instruct analysis of ssp. xantiana and parviflora. Right: Ancestral geography analysis showing allopatric parviflora popns as most ancestral.
In sympatry, reproductive isolation is conferred primarily by floral traits and flowering phenology (Briscoe Runquist et al. 2014). In both directions, total reproductive isolation exceeds 98% despite the ability to successfully cross these taxa. This work has emphasized the importance of premating and postmating-prezygotic barriers for the maintenance of these recently diverged lineages.
There is also a partial crossing barrier, where crosses from the selfer to the outcrosser result in fewer seeds than the reverse cross. Few hybrids are formed in the field, although the taxa are partially cross-compatible. We have detected introgression at the molecular level that is asymmetric and that varies considerably in magnitude among geographically disparate contact zones (Pettengill and Moeller 2012b).
We have also discovered a strong pattern of reproductive character displacement, particularly in the selfer (parviflora). The most ancestral, eastern parviflora populations are larger-flowered, with traits that allow for some outcrossing, whereas the recently derived western populations have highly reduced flowers that almost exclusively self-fertilize.
We are currently testing the hypothesis that this pattern of reproductive character displacement is the result of reinforcement. Reinforcement refers to the process whereby natural selection causes exaggerated divergence in traits that influence mating in sympatry because that divergence minimizes the costly formation of hybrids.
Sianta, S.A., S. Peischl, D.A. Moeller, & Y. Brandvain. Genetic load may increase or decrease with selfing depending upon the recombination environment. Evolution, accepted. doi.org/10.1101/2021.05.20.445016.
Ruane, L.G., S.M. Mangum, K.M. Horner, & D.A. Moeller. 2020. The opportunity for outcrossing varies across the geographic range of the primarily selfing Clarkia xantiana ssp. parviflora. American Journal of Botany, in press.
Briscoe Runquist, R.D., M.A. Geber, M. Pickett-Leonard, & D.A. Moeller. 2017. Mating system evolution under strong pollen limitation: Evidence of disruptive selection through male and female fitness in Clarkia xantiana. American Naturalist 189:549-563.
Pettengill, J.B., R.D. Briscoe Runquist, & D.A. Moeller. 2016. Mating system divergence affects the distribution of sequence diversity within and among populations of recently diverged subspecies of Clarkia xantiana (Onagraceae). American Journal of Botany 103:99-109.
Briscoe Runquist, R.D., E. Chu†, J.L. Iverson†, J.C. Kopp†, & D.A. Moeller. 2014. Rapid evolution of reproductive isolation between incipient outcrossing and selfing Clarkia species. Evolution 68:2885-2900.
Briscoe Runquist, R.D. & D.A. Moeller. 2014. Floral and mating system divergence in secondary sympatry: testing an alternative hypothesis to reinforcement in Clarkia. Annals of Botany 100:1916-1921.
Pettengill, J.B., & D.A. Moeller. 2012b. Phylogeography of speciation: allopatric divergence and secondary contact between outcrossing and selfing Clarkia. Molecular Ecology 21:4578-4592.
Pettengill, J.B., & D.A. Moeller. 2012a. Tempo and mode of mating system evolution between incipient Clarkia species. Evolution 66:1210-1225.