Low genetic structure in a bat-pollinated, extinct megafauna-dispersed, tropical tree species (Crescentia alata) from Western Mexico

Background/Question/Methods

The genetic structure of plant populations is shaped by pollen and seed dispersal, and by landscape features that influence those processes. We examined the fine-scale genetic structure of populations of Crescentia alata, a tropical dry forest tree species that is pollinated by bats, and which were purportedly dispersed by megafaunal seed dispersers that went extinct in the Pleistocene. If no other seed dispersal vector is present to move these hard-to-open fruit, we might expect the loss of the original dispersal agent to create highly localized genetic structure. To assess genetic structure, we developed 8 neutral microsatellite markers de novo for C. alata, and genotyped 161 trees sampled from 16 localities across a geographic region of 92,000 hectares around the Chamela-Cuixmala Biosphere Reserve in Jalisco, Mexcio. We used a Bayesian clustering program to detect the number of possible subpopulations. We then compared the genetic and geographic distances among the sites and looked for evidence of isolation by distance. Finally, we tested the central hypothesis that the loss of historical seed dispersal agent results in restricted dispersal by quantifying the patterns of spatial autocorrelation at broad and fine geographic scales.

Results/Conclusions

Our STRUCTURE analysis identified two North-South genetic clusters, and we found low but significant genetic structure between these two regions (F_RT = 0.019), and higher structure between sampling localities (F_ST = 0.049). We found evidence for isolation by distance between sites, at a large geographic scale. We observed significant spatial autocorrelation at a broad scale (0-12km) with low kinship coefficients at these distance classes (0.08 > r > 0.027). Although the fine scale spatial autocorrelation was significant (0-800m, 0.030 > r > 0.106), it did not reveal the degree of spatial clustering that would be apparent for a species that is “missing” its dispersal agent. We conclude that the overall low level of genetic structure of C. alata trees across our study region suggests that gene flow is largely unrestricted, and the lack of strong fine scale genetic structure indicates a dispersal vector other than gravity. Instead, high pollen flow via bat pollinators is a plausible mechanism causing the homogenization of genetic diversity of C. alata trees in this region. In addition, the flooding of arroyos during the rainy season may promote long-distance gene flow via seeds, and contribute to this pattern of low levels of relatedness across large distances.