Limited Pollen Dispersal Contributes to Population Genetic Structure but Not Local Adaptation in Quercus oleoides Forests of Costa Rica

Abstract

Background Quercus oleoides Cham. and Schlect., tropical live oak, is a species of conservation importance in its southern range limit of northwestern Costa Rica. It occurs in high-density stands across a fragmented landscape spanning a contrasting elevation and precipitation gradient. We examined genetic diversity and spatial genetic structure in this geographically isolated and genetically distinct population. We characterized population genetic diversity at 11 nuclear microsatellite loci in 260 individuals from 13 sites. We monitored flowering time at 10 sites, and characterized the local environment in order to compare observed spatial genetic structure to hypotheses of isolation-by-distance and isolation-by-environment. Finally, we quantified pollen dispersal distances and tested for local adaptation through a reciprocal transplant experiment in order to experimentally address these hypotheses.ResultsHigh genetic diversity is maintained in the population and the genetic variation is significantly structured among sampled sites. We identified 5 distinct genetic clusters and average pollen dispersal predominately occurred over short distances. Differences among sites in flowering phenology and environmental factors, however, were not strictly associated with genetic differentiation. Growth and survival of upland and lowland progeny in their native and foreign environments was expected to exhibit evidence of local adaptation due to the more extreme dry season in the lowlands. Seedlings planted in the lowland garden experienced much higher mortality than seedlings in the upland garden, but we did not identify evidence for local adaptation.ConclusionOverall, this study indicates that the Costa Rican Q. oleoides population has a rich population genetic history. Despite environmental heterogeneity and habitat fragmentation, isolation-by-distance and isolation-by-environment alone do not explain spatial genetic structure. These results add to studies of genetic structure by examining a common, tropical tree over multiple habitats and provide information for managers of a successional forest in a protected area.

Natural selection and neutral evolutionary processes contribute to genetic divergence in leaf traits across a precipitation gradient in the tropical oak Quercus oleoides

“…A thorough phenotypic characterization was carried out in seedlings of Q. oleoides growing in two common garden experiments under natural and controlled conditions. These gardens were part of a network of experiments established over a decade within the native range of the species in several countries of Central America complemented by greenhouse experiments at the University of Minnesota to test for local adaptation and population‐level variation in this tropical oak (see Cavender‐Bares & Ramírez‐Valiente ; Cavender‐Bares , ; Center ; Center et al., ; Deacon & Cavender‐Bares, ; Koehler, Center, & Cavender‐Bares, , Ramírez‐Valiente, Koehler et al., ; Ramírez‐Valiente et al., ). In this study, we used the most complete common garden experiments of the series, which included populations from across the entire species distribution and climatic range and had well‐replicated family structure.…”

“…We extracted DNA using Qiagen DNeasy Plant Mini Kits from 52 individuals from four populations of Q. oleoides and amplified eleven previously published microsatellite loci: Qp ZAG 1/2, Qp ZAG 1/5, Qp ZAG 9, Qp ZA15, Qp ZAG 16, Qp ZAG 36, Qp ZAG 46, Qp ZAG 102, Qp ZAG 110 (Steinkellner, Lexer, Turetschek, & Glössl, ), Qr ZAG 11 and Qr ZAG 30 (Kampfer, Lexer, Glössl, & Steinkellner, ). Those data were combined with previously published data from 166 individuals for the same set of microsatellites (Cavender‐Bares et al., , ; Deacon & Cavender‐Bares, ). In total, we had the genotypes of 218 individuals from ten Q. oleoides populations (9–41 individuals per population, Table ).…”

“…First, this species is widely distributed across a high variety of precipitation regimes in seasonally dry tropical forests of Central America (Cavender‐Bares et al., ). Second, intraspecific differences have been previously reported in traits such as germination, growth, photoprotective pigments, morphology, physiology and survival (Cavender‐Bares, Sack, & Savage, , Cavender‐Bares, Gonzalez‐Rodríguez, Pahlich, Koehler, & Deacon, ; Center, Etterson, Deacon, & Cavender‐Bares, ; Deacon & Cavender‐Bares, ; Ramírez‐Valiente, Koehler, & Cavender‐Bares, ; Ramírez‐Valiente, Valladares, Delgado, Nicotra, & Aranda, ; Ramírez‐Valiente & Cavender‐Bares, ; Ramírez‐Valiente et al., ). Third, the species exhibits a complex evolutionary history with a clear genetic disjunction in neutral molecular markers between southern populations and population from the rest of the distribution range (Cavender‐Bares et al., , ).…”

“…Previous studies have suggested that Costa Rican populations of Q. oleoides diverged from the Central American widespread population about 1.9 Ma (±0.5) as a result of the formation of the Nicaraguan depression and associated volcanic activity causing barriers to gene flow (Cavender‐Bares et al., , ; Deacon & Cavender‐Bares, ). Results from organelle genetic markers showed a single chloroplast haplotype in Costa Rica and also supported the idea of long‐term isolation of this population (Cavender‐Bares et al., , ).…”

Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution

“…The Costa Rican and Honduran populations are estimated to have diverged 1.9 Ma (1.0–3.1 Ma; Cavender‐Bares et al ., ). In four separate experiments, where both seeds or seedlings from known mothers were planted in a random block design (Center, ; Deacon & Cavender‐Bares, ; Center et al ., ; Ramírez‐Valiente et al ., ), we found no evidence of local adaptation at either early germination stages or after multiple years of growth across major precipitation gradients. Rather, all populations tended to perform better in climates with less severe dry seasons (Center, ; Deacon & Cavender‐Bares, ; Cavender‐Bares & Ramírez‐Valiente, ; Ramírez‐Valiente et al ., ).…”