J. L. Hamrick’s research while affiliated with University of Georgia and other places

The tree species on Barro Colorado Island (BCI) differ widely in their relative abundance and various life-history traits, including mating systems, pollen- and seed-dispersal syndromes, and genetic diversity. BCI researchers have been at the fore front of basic research in understanding the origin and maintenance of genetic diversity in tropical tree populations using innovative and state-of-the-art tools across the past 40 years. These studies have examined the role of evolutionary processes, including genetic drift, gene flow via seed and pollen, mating systems, and natural selection in shaping the genetic diversity and population genetic structure of tree populations. Here, we provide a short history and main findings of eco-evolutionary and population genetic research conducted on the island and nearby mainland. We then outline future areas of research that could further unite ecological and evolutionary research on BCI in the coming century. </p

The dispersal and colonization of plant populations allow species to occupy novel habitats, migrate, and undergo range shifts in response to changing environmental factors and, as such, are fundamental ecological processes for ensuring the long‐term persistence of species. Natural landscape disturbance often generates habitats available for colonization. Patterns of colonization and population expansion can be inferred from the levels and partitioning of genetic variation of plant populations with known disturbance histories, such as recent volcanic eruptions. We sampled and mapped 496 individuals from two populations of the colonizing terrestrial orchid, Sobralia chrysostoma , on the 1992 lava flow of Volcán Arenal in central Costa Rica. We used neutral co‐dominant markers to genotype individuals and estimate population genetic statistics. Both populations had high mean levels of genetic diversity ( P = 100%; AP = 3.31; H e = 0.259) suggesting that the lava flow was colonized by numerous individuals that likely originated from multiple source populations. However, significant spatial genetic structure (SGS) was only present in one population at the smallest distance class (≤2 m) and was low ( r = 0.032). That these large and genetically diverse populations had such low SGS and an absence of SGS, respectively is contrary to expectations and differs significantly from the pattern in Epidendrum radicans (Orchidaceae), with which S. chrysostoma is growing sympatrically. Our results suggest that these two populations either consist primarily of immigrant individuals or that seeds produced in situ dispersed over longer distances, thereby producing larger seed shadows and greater overlap of seed shadows.

Colonization is a fundamental ecological process that is important for the persistence of species, particularly when a changing environment necessitates range shifts. Vacant habitats available for colonization often arise from landscape disturbance. Colonization and population expansion processes can be inferred by examining the levels and spatial distribution of genetic variation of plant populations with known disturbance histories. Samples (N = 690) of the terrestrial orchid, Epidendrum radicans, were collected from five lava flow sites on the slopes of Volcán Arenal in Costa Rica that last experienced major eruptions in 1968 and 1992. Individuals were also sampled (N = 188) from four regional populations. Samples were characterized using 15 nuclear genetic markers and analyzed using population genetics statistics. Genetic diversity within sites was moderate (He = 0.092–0.192). Contrary to expectation, diversity tended to be lower on the older lava flows (0.131 vs. 0.172) which may reflect their more sheltered topography that restricted pollen/seed immigration, and/or greater intra- and interspecific competition. Genetic diversity measures indicate that the lava flows were colonized by numerous individuals that likely originated from multiple sources while spatial genetic structure (SGS) statistics indicate that most recruitment in the study sites subsequent to colonization resulted from in situ reproduction and localized seed deposition. Younger sites had significantly greater SGS over larger distances which reflects fewer reproductive events, and less spatial and temporal overlap of seed shadows relative to the older sites. Clones were also generally smaller on the younger sites (≤3 m vs. ≤8 m).

The slender wild oat ( Avena barbata ) was widely studied in California using allozymes in the 1970s and interpreted as a case of ecotypic adaptation to contrasting moisture environments. However, common garden studies suggested that the moist-associated (“mesic”) ecotype had high fitness in both moist and dry habitats, thus predicting an adaptive spread into areas occupied by the dry associated (“xeric”) ecotype. To test this prediction, we revisited 100 populations of A. barbata that were screened genetically 40 y ago. As expected, mesic allozyme and morphological markers are much more common than in the 1970s. The less-fit xeric ecotype, while still widespread, has declined markedly in range and frequency. Genotyping by sequencing of modern populations reveals striking genetic uniformity within each of the two ecotypes. In recombinants between the two ecotypes, the mesic allele at a major fitness quantitative trait locus (QTL) shows a high frequency but so do many other genomic regions not identified as fitness QTL. Additional introduced genotypes are diverse and more widespread than in the past, and our results show that these have spread into the former range of the xeric ecotype to an even greater extent than the mesic ecotype has. While these results confirm the prediction of contemporary evolution from common gardens, they also suggest that much of the change has been driven by additional waves of introduced genotypes.

Dispersal and colonization are among the most important ecological processes for species persistence as they allow species to track changing environmental conditions. During the last glacial maximum (LGM), many cold-intolerant Northern Hemisphere plants retreated to southern glacial refugia. During subsequent warming periods, these species expanded their ranges northward. Interestingly, some tree species with limited seed dispersal migrated considerable distances after the LGM ~19,000 years before present (YBP). It has been hypothesized that indigenous peoples may have dispersed valued species, in some cases beyond the southern limits of the Laurentide Ice Sheet. To investigate this question, we employed a molecular genetics approach on a widespread North American understory tree species whose fruit was valued by indigenous peoples. Twenty putative anthropogenic (near pre-Columbian habitations) and 62 wild populations of Asimina triloba (pawpaw), which produces the largest edible fruit of any North American tree, were genetically assayed with nine microsatellite loci. Putative anthropogenic populations were characterized by reduced genetic diversity and greater excess heterozygosity relative to wild populations. Anthropogenic populations in regions that were glaciated during the LGM had profiles consistent with founder effects and reduced gene flow, and shared rare alleles with wild populations hundreds of kilometers away (mean = 723 km). Some of the most compelling evidence for human-mediated dispersal is that putative anthropogenic and wild populations sharing rare alleles were separated by significantly greater distances (mean = 695 km) than wild populations sharing rare alleles (mean = 607 km; p = .014). Collectively, the genetic data suggest that long-distance dispersal played an important role in the distribution of pawpaw and is consistent with the hypothesized role of indigenous peoples.

Aim Predictions of species' responses to accelerating global climate change require an understanding of historical range shifts. However, large‐scale phylogeographical studies of Eastern North American understorey plant taxa are relatively scarce. Here we employ ecological niche modelling and genetic analyses for inference of optimal pawpaw habitat in the past and future. Location In all, 26 states in the eastern United States. Taxon Asimina triloba (L.) Dunal (Annonaceae). Methods The present‐day niche of Asimina triloba was modelled in Maxent using seven bioclimatic variables, elevation and location data from field samples and herbarium specimens. To model historically optimal habitats, the present‐day model was projected onto rasters of seven bioclimatic variables and elevation representing the last glacial maximum (~22,000 years before present [YBP]) and the mid‐Holocene (~6,000 YBP). Predicted habitat suitability for 2070 was also modelled. Additionally, 62 populations were genotyped with nine nuclear microsatellite loci and statistically analysed. Levels and partitioning of genetic variation within and among populations were estimated within a geographical context. Results Models indicate that optimal habitat 22,000 YBP was severely restricted to mostly now‐submerged Gulf of Mexico and southeastern US coastlines. By 2070, models suggest that optimal habitat will expand substantially northward relative to the present. Species‐level genetic diversity (HE = 0.765) was high and genetic structure among populations was moderate (GST = 0.202). Structure indicates that there are two population clusters straddling the Appalachian Mountains. Main conclusions Models suggest that 22,000 YBP A. triloba was restricted to two major refugia in narrow bands of mostly now‐submerged habitat and possibly several small inland refugia. Molecular data are consistent suggesting that the eastern refugia expanded to give rise to the eastern cluster which is characterized by higher genetic diversity. The Gulf of Mexico refugium likely gave rise to populations in the western cluster, which is characterized by lower genetic diversity.

Reviews that summarize the genetic diversity of plant species in relation to their life history and ecological traits show that forest trees have more genetic diversity at population and species levels than annuals or herbaceous perennials. In addition, among‐population genetic differentiation is significantly lower in trees than in most herbaceous perennials and annuals. Possible reasons for these differences between trees and herbaceous perennials and annuals have not been discussed critically. Several traits, such as high rates of outcrossing, long‐distance pollen and seed dispersal, large effective population sizes (Ne), arborescent stature, low population density, longevity, overlapping generations, and occurrence in late successional communities, may make trees less sensitive to genetic bottlenecks and more resistant to habitat fragmentation or climate change. We recommend that guidelines for genetic conservation strategies be designed differently for tree species versus other types of plant species. Because most tree species fit an LH scenario (low [L] genetic differentiation and high [H] genetic diversity), tree seeds could be sourced from a few populations distributed across the species’ range. For the in situ conservation of trees, translocation is a viable option to increase Ne. In contrast, rare herbaceous understory species are frequently HL (high differentiation and low diversity) species. Under the HL scenario, seeds should be taken from many populations with high genetic diversity. In situ conservation efforts for herbaceous plants should focus on protecting habitats because the typically small populations of these species are vulnerable to the loss of genetic diversity. The robust allozyme genetic diversity databases could be used to develop conservation strategies for species lacking genetic information. As a case study of reforestation with several tree species in denuded areas on the Korean Peninsula, we recommend the selection of local genotypes as suitable sources to prevent adverse effects and to insure the successful restoration in the long term.

Eastern white pine (Pinus strobus L.) is a widespread conifer in eastern North America. A novel dieback phenomenon, as well as increasing global temperatures contributing to the contraction of suitable habitat, is threatening this species’ long-term persistence in the Southern Appalachian Mountains. This southern extent of its current range is where P. strobus is hypothesized to have survived in refugial populations during the last glacial maximum. As a result, extant populations located here may have higher levels of ancestral genetic diversity, and by extension, adaptive potential. We genotyped 432 P. strobus individuals from 23 sites throughout the Southern Appalachians and another 34 individuals from two reference populations in the northern USA, using 10 established microsatellite markers. Levels of genetic diversity in the southern portion of the range were comparable but not higher than reference northern populations. There was an overall heterozygote deficiency and high inbreeding coefficient (FIS = 0.173); however, these values were comparable to published research of P. strobus throughout the northern range. There was low overall genetic differentiation (FST = 0.055) among populations in the Southern Appalachians and population structure was best explained by ecoregions. These results show that P. strobus in the Southern Appalachians is a fairly heterogenous and admixed species with relatively high genetic diversity mostly partitioned within populations. The Southern Appalachians remains an important area for P. strobus conservation, but not necessarily because it is genetically unique.

Spatial patterns of genetic variation can reveal otherwise cryptic evolutionary and landscape processes. In northwestern Costa Rica, an approximately concordant genetic discontinuity occurs among populations of several plant species. We conducted phylogeographic analyses of an epiphytic orchid, Brassavola nodosa, to test for genetic discontinuity and to explore its underlying causes. We genotyped 18 populations with 19 nuclear loci and two non-coding chloroplast sequence regions. We estimated genetic diversity and structure, relative importance of pollen and seed dispersal, and divergence time to understand how genetic diversity was spatially partitioned. Nuclear genetic diversity was high with little differentiation among populations (GSTn = 0.065). In contrast, chloroplast haplotypes were highly structured (GSTc = 0.570) and reveal a discontinuity between northwestern and southeastern populations within Costa Rica. Haplotype differences suggest two formerly isolated lineages that diverged ~10,000–100,000 YBP. Haplotype mixing and greater genetic diversity occur in an intermediate transition zone. Patterns of nuclear and chloroplast data were consistent. Different levels of genetic differentiation for the two genomes reflect the relative effectiveness of biotic versus abiotic dispersers of pollen and seeds, respectively. Isolation of the two lineages likely resulted from the complex environmental and geophysical history of the region. Our results suggest a recent cryptic seed dispersal barrier and/or zone of secondary contact. We hypothesize that powerful northeasterly trade winds hinder movement of wind-borne seeds between the two regions, while the multi-directional dispersal of pollen by strong-flying sphinx moths resulted in lower differentiation of nuclear loci.