Interspecific gene flow in a multispecies oak hybrid zone in the Sierra Tarahumara of Mexico

Abstract

Background and aims: Interspecific gene flow can occur in many combinations among species within the genus Quercus, but simultaneous hybridization among more than two species has been rarely analysed. The present study addresses the genetic structure and morphological variation in a triple hybrid zone formed by Q. hypoleucoides, Q. scytophylla and Q. sideroxyla in north-western Mexico.

Methods: A total of 247 trees from ten reference and 13 presumed intermediate populations were characterized using leaf shape variation and geometric morphometrics, and seven nuclear microsatellites as genetic markers. Discriminant function analysis was performed for leaf shape variation, and estimates of genetic diversity and structure, and individual Bayesian genetic assignments were obtained.

Key results: Reference populations formed three completely distinct groups according to discriminant function analysis based on the morphological data, and showed low, but significant, genetic differentiation. Populations from the zone of contact contained individuals morphologically intermediate between pairs of species in different combinations, or even among the three species. The Bayesian admixture analysis found that three main genetic clusters best fitted the data, with good correspondence of reference populations of each species to one of the genetic clusters, but various degrees of admixture evidenced in populations from the contact area.

Conclusions: The three oak species have formed a complex hybrid zone that is geographically structured as a mosaic, and comprising a wide range of genotypes, including hybrids between different species pairs, backcrosses and probable triple hybrids.

Fig. 1.

Geographical distribution of the three red-oak species studied, Quercus scytophylla, Q. hypoleucoides and Q. sideroxyla.

Fig. 2.

Map showing sampling localities representing parental and intermediate populations. Each pie chart represents the proportions in each population of the three genetic groups as assigned by the program STRUCTURE. Green, red and blue represent the genetic groups corresponding to Quercus scytophylla, Q. sideroxyla and Q. hypoleucoides, respectively. Numbers next to each symbol correspond to the population numbers given in Table 1. The area of species contact is delineated with a dashed rectangle.

Fig. 3.

Scatterplot of individual scores from discriminant function analysis of populations in the oak complex based on foliar geometric morphometric data. Closed circles, squares and triangles symbolize representative populations of Quercus scytophylla, Q. hypoleucoides and Q. sideroxyla, respectively, and open circles and crosses are the Mixed 1 and Mixed 2 population groups, respectively. See text for details.

Fig. 4.

(A) Mean and standard deviation of lnP(D) for ten independent runs of STRUCTURE plotted against the number of genetic groups (K) used in the analysis. (B) Values of ΔK plotted against K. In both cases the peak indicates the most probable number of genetic groups given the data.

Fig. 5.

Genetic assignment of individuals and populations according to the Bayesian method implemented in the program STRUCTURE. One sample, considered to explain the data best, of ten iterated runs is shown. Each thin horizontal line represents an individual and the proportion of each colour is the proportion of ancestry derived from each of the three main genetic groups (K = 3) inferred. Populations are separated by black lines. Values of the proportions of ancestry for each population are given in the table.

Fig. 6.

Frequency of the different genotypic classes observed in each population. Individuals were assigned to each category (Q. scytophylla, Q. hypoleucoides, Q. sideroxyla, hybrids between Q. scytophylla and Q. sideroxyla, hybrids among Q. scytophylla × Q. hypoleucoides, hybrids between Q. sideroxyla and Q. hypoleucoides and triple hybrids, as indicated in the key), depending on their individual coefficient of admixture derived from STRUCTURE. Performance of the assignment procedure was previously assessed by analysing simulated genotypes (see text for details).