Reproductive Patterns Shape Introgression Dynamics and Species Succession Within the European White Oak Species Complex

Abstract

The reproductive system of hybrids is an important factor shaping introgression dynamics within species complexes. We combined paternity and parentage analyses with previous species characterization by genetic assignment, to directly identify reproductive events that occurred within a stand comprising four European white oak species. Comparing species status of parent pairs provided a precise quantification of hybridization rate, backcrosses, and intraspecific matings in two life stages. The detailed mating system analysis revealed new findings on the dynamics of interspecific gene flow. First, hybrids acted successfully as both male and female during reproduction. They produced acorns and seedlings that were as viable as those sired by purebreds. Second, species maintenance could be due to a relatively low level of interspecific mating contrasting with a large proportion of intraspecific crosses and backcrosses. Despite a high proportion of hybrids and extensive interspecific gene flow, partial species integrity is maintained by genetically controlled pollen discrimination, ensuring preferential matings within purebreds and high parental species fidelity in hybrid reproduction, which impedes complete collapse into a continuous hybrid swarm. Finally, we showed that pollen from the different species had unequal contributions to reproduction suggesting that introgression processes could ultimately lead to extirpation or expansion of some species.

Genetic evidence of reproductive isolation in a remote enclave of Quercus pubescens in the presence of cross-fertile species

“…On the contrary, we observed that relatively young individuals start to produce acorns. Also, our results did not support an increased selffertilisation rate, as our estimate of the contemporary selfing rate equalled 2%, which is comparable with other findings for European white oaks in the main species range (Streiff et al 1999;Curtu et al 2009; Burczyk 2010; Lepais and Gerber 2011). It seems that the study population produced enough pollen to maintain cross-pollination, and/or some pre-or post-zygotic mechanisms (Buschbom et al 2011) prevent more intense inbreeding.…”

“…In European white oaks effective pollen dispersal is usually bimodal, as a result of limited pollen dispersal within a population and a large pollen immigration from outside (e.g. Streiff et al 1999;Salvini et al 2009;Chybicki and Burczyk 2010;Buschbom et al 2011;Lepais and Gerber 2011). However, due to very low effective pollen immigration (as our results suggest), in the study population a distribution of mating distances can be unimodal with a peak at short distances.…”

“…The earlier surveys of leaf morphology suggested that trees in the study population reveal great variation spanning among three species: Q. pubescens, Q. petraea and Q. robur (Celiński and Filipek 1958;Staszkiewicz 1977;Danielewicz et al 2002). However, because these species are potentially cross-fertile (Lepais et al 2009;Salvini et al 2009;Lepais and Gerber 2011), we assumed that the study population embraces all 2,200 individuals, which however can mate non-randomly due to taxonomic or other barriers (e.g. distance, flowering synchrony).…”

“…Given that the study stand is a mixture of three oak species, it becomes evident that the population of Q. pubescens in Bielinek is being exposed to inter-specific pollen and subjected to a strong pressure of introgression, which seems to be stronger than within previously studied populations of the species complex (e.g. Finkeldey 2001;Curtu et al 2007Curtu et al , 2009Salvini et al 2009;Lepais et al 2009;Lepais and Gerber 2011). Although the introgression from Q. petraea could be the case, accompanying or alternative processes such as genetic drift and/or selection at the extremes of species ecological spectrum cannot be definitely excluded.…”

“…A common observation is that a few tens percent of acorns result from pollination with immigrating pollen (e.g. Streiff et al 1999;Curtu et al 2009;Lepais and Gerber 2011;Buschbom et al 2011), and the immigration rate is relatively stable at the stage of established seedlings (Chybicki and Burczyk 2010;Lepais and Gerber 2011). This suggests that the population of Q. pubescens in Bielinek should experience a permanent oak pollen flow from the outside as well.…”