John D. Nason

Landscape approaches to historical and contemporary gene flow in plants.

Growing interest in metapopulation dynamics and dispersal at a landscape level is promoting new approaches to the study of contemporary gene flow. These approaches have been fostered by the development of new genetic markers and statistical methods, as well as an awareness that contemporary gene flow cannot be reliably estimated by conventional methods based on genetic structure. Estimation of the spatial and temporal dynamics of pollen and seed movement with respect to extant landscape features can aid evolutionary and conservation biologists in predicting the demographic and genetic responses of species to naturally occurring or human-mediated population subdivision.

The influence of seed dispersal mechanisms on the genetic structure of tropical tree populations

Seed dispersal mechanisms should have a direct impact on the genetic structure of populations. Species whose seeds are dispersed near the maternal plant (e.g. gravity or wind dispersal) or species whose seeds are deposited in clumps or patches should have more fine-scale genetic structure than species whose seeds are dispersed singly by mobile animals. Furthermore, due to the overlap of seed shadows, species with high adult densities should have less genetic structure than species with lower densities. Allozyme analyses of three tropical tree species belonging to the moist tropical forest of Barro Colorado Island, Republic of Panama, were used to describe variation in the scale and intensity of genetic structure within their populations. The genetic structure of seedlings and immature trees in the low-density, wind-dispersed species (Platypodium elegans) was the coarsest and strongest whereas genetic structure in a population of Swartzia simplex var. ochnacea (high density, bird-dispersed) was both the finest and the weakest. The genetic structure of Alseis blackiana, a high-density, wind-dispersed species was intermediate in both degree and scale. In P. elegans and A. blackiana, which had ‘J’ shaped size distributions, the significant genetic structure seen in the smaller and intermediate diameter classes disappeared in the largest diameter class. The loss of genetic structure was not observed in S. simplex, a species with a more even size distribution.

The breeding structure of a tropical keystone plant resource

Despite the recognized importance of maintaining viable populations of keystone plant resources in tropical wildlife parks and forested preserves, the critical question of what constitutes effective breeding units of these species has not been directly addressed. Here we use paternity analysis techniques to reconstruct the genotypes of pollen donor trees and to estimate pollen dispersal distances and breeding population size parameters for Panamanian populations of seven species of monoecious strangler figs (Ficus, Moraceae), a particularly widespread and influential group of keystone producers. Despite the minute size (1–2 mm) and short lifespan (2–3 d) of the species-specific wasp pollinators (Agaonidae, Chalcidoidea), pollen dispersal was estimated to occur routinely over distances of 5.8–14.2 km between widely spaced host trees. As a result of such extensive pollen movement, breeding units of figs comprise hundreds of intermating individuals distributed over areas of 106–632 km2, an order of magnitude larger than has been documented for any other plant species. Moreover, these results should be generalizable to the 350 or so monoecious fig species that share this pollination system. The large areal extent of breeding units of these keystone plant resources has important implications for our understanding of both the evolution of tropical biodiversity and its maintenance by applied conservation efforts.

SPATIAL POPULATION GENETIC STRUCTURE IN TRILLIUM GRANDIFLORUM: THE ROLES OF DISPERSAL, MATING, HISTORY, AND SELECTION

Abstract.— The roles of the various potential ecological and evolutionary causes of spatial population genetic structure (SPGS) cannot in general be inferred from the extant structure alone. However, a stage‐specific analysis can provide clues as to the causes of SPGS. We conducted a stage‐specific SPGS analysis of a mapped population of about 2000 Trillium grandiflorum (Liliaceae), a long‐lived perennial herb. We compared SPGS for juvenile (J), nonreproductive (NR), and reproductive (R) stages. Fishers exact test showed that genotypes had Hardy‐Weinberg frequencies at all loci and stage classes. Allele frequencies did not differ between stages. Bootstrapped 99% confidence intervals (99%CI) indicate that F‐statistic values are indistinguishable from zero, (except for a slightly negative F1T for the R stage). Spatial autocorrelation was used to calculate f, the average kinship coefficient between individuals within distance intervals. Null hypothesis 99%CIs for f were constructed by repeatedly randomizing genotypic locations. Significant positive fine‐scale genetic structure was detected in the R and NR stages, but not in the J stage. This structure was most pronounced in the R stage, and declined by about half in each remaining stage: near‐neighbor f= 0.122, 0.065, 0.027, for R, NR, and J, respectively. For R and NR, the near‐neighbor f lies outside the null hypothesis 99%CI, indicating kinship at approximately the level of half‐sibs and first cousins, respectively. We also simulated the expected SPGS of juveniles post dispersal, based on measured R‐stage SPGS, the mating system, and measured pollen and seed dispersal properties. This provides a null hypothesis expectation (as a 99%CI) for the J‐stage correlogram, against which to test the likelihood that post‐dispersal events have influenced J‐stage SPGS. The actual J correlogram lies within the null hypothesis 99%CI for the shortest distance interval and nearly all other distance intervals indicating that the observed low recruitment, random mating and seed dispersal patterns are sufficient to account for the disappearance of SPSG between the R and the J stages. The observed increase in SPGS between J and R stages has two potential explanations: history and local selection. The observed low total allelic diversity is consistent with a past bottleneck: a possible historical explanation. Only a longitudinal stage‐specific study of SPGS structure can distinguish between historical events and local selection as causes of increased structure with increasing life history stage.

HOST-ASSOCIATED GENETIC DIFFERENTIATION IN PHYTOPHAGOUS INSECTS: GENERAL PHENOMENON OR ISOLATED EXCEPTIONS? EVIDENCE FROM A GOLDENROD-INSECT COMMUNITY

Abstract There is growing awareness of the importance of natural selection in driving genetic divergence and speciation, and several of the most apparent cases of this ecological speciation are provided by the existence of genetically distinct host forms in phytophagous insects. Such examples of host‐associated differentiation (HAD) have become increasingly documented, and the implications of this phenomenon for the diversification of insects are becoming widely appreciated. However, instances of HAD remain rare relative to insect diversity and are sparsely distributed both ecologically and taxonomically. We sought to assess the frequency of HAD in a model herbivore community by examining genetic divergence in a variety of herbivores that feed on two closely related and broadly sympatric species of goldenrod (Solidago altissima and S. gigantea). Using mitochondrial DNA and allozyme data, in conjunction with previously published studies, we found that four of nine herbivores exhibited evidence of HAD, including possible host races or cryptic species. Using a range of reasonable substitution rate estimates for cytochrome oxidase I mitochondrial DNA, we found that HAD appears to have proceeded asynchronously across taxa. This pattern, along with the broadly sympatric distribution of host plants and the specialized life histories of the phytophagous insects, is consistent with sympatric divergence in some or all of these taxa. Although further behavioral and ecological study is needed, our survey of HAD in a community of herbivores indicates that ecological (perhaps sympatric) speciation may have been responsible for generating a significant fraction of the extant diversity of phytophagous insects.

Landscape modelling of gene flow: improved power using conditional genetic distance derived from the topology of population networks

Landscape genetics is a burgeoning field of interest that focuses on how site‐specific factors influence the distribution of genetic variation and the genetic connectivity of individuals and populations. In this manuscript, we focus on two methodological extensions for landscape genetic analyses: the use of conditional genetic distance (cGD) derived from population networks and the utility of extracting potentially confounding effects caused by correlations between phylogeographic history and contemporary ecological factors. Individual‐based simulations show that when describing the spatial distribution of genetic variation, cGD consistently outperforms the traditional genetic distance measure of linearized FST under both 1‐ and 2‐dimensional stepping stone models and Cavalli‐Sforza and Edward’s chord distance Dc in 1‐dimensional landscapes. To show how to identify and extract the effects of phylogeographic history prior to embarking on landscape genetic analyses, we use nuclear genotypic data from the Sonoran desert succulent Euphorbia lomelii (Euphrobiaceae), for which a detailed phylogeographic history has previously been determined. For E. lomelii, removing the effect of phylogeographic history significantly influences our ability to infer both the identity and the relative importance of spatial and bio‐climatic variables in subsequent landscape genetic analyses. We close by discussing the utility of cGD in landscape genetic analyses.

HISTORICAL VICARIANCE AND POSTGLACIAL COLONIZATION EFFECTS ON THE EVOLUTION OF GENETIC STRUCTURE IN LOPHOCEREUS, A SONORAN DESERT COLUMNAR CACTUS

Abstract.— Distinguishing the historical effects of gene migration and vicariance on contemporary genetic structure is problematic without testable biogeographic hypotheses based on preexisting geological and environmental evidence. The availability of such hypotheses for North Americas Sonoran Desert has contributed to our understanding of the effect of historical vicariance and dispersal events on the diversification of this regions vertebrate biota but have not yet been applied to its flora. In this paper we describe a detailed allozyme analysis of the population genetic structure and phylogeography of the Sonoran Desert columnar cactus, Lophocereus schottii (senita). Inferred phylogroup distributions reflect two historical vicariance events: (1) a middle Pliocene northward transgression of the Sea of Cortez that is reflected in well‐supported Baja California peninsular and continental phylogroups but not in current taxonomic treatments of the species; and (2) a late Pliocene transpeninsular seaway across southern Baja that is reflected in tentative support for peninsular and southern Cape Region phylogroups corresponding to taxonomic varietiesL. schottii var. schottii and L. schottii var. australis, respectively. A middle Pleistocene midpeninsular seaway hypothesized to explain congruent phylogroup distributions in several vertebrate taxa is not reflected in L. s. var. schottii, nor is the distinction of a third variety, L. s. var. tenuis, from continental populations ofL. s. var. schottii. Linear regression of pairwise estimates of interpopulation differentiation (Ḿ and FST/[1 – FST]) on interpopulation geographic distance revealed significant evidence of isolation by distance within peninsular and continental phylogroups but not between them, consistent with historical vicariance between but not within these regions. We also found significant evidence of isolation by distance between putative L. s. var. schottii and L. s. var. australis phylogroups, suggesting that reproductive isolation between peninsular and Cape Region forms is incomplete. Within peninsular, but not continental, phylogroups, northward range expansion from southern Pleistocene refugia is reflected in significant declines in genetic variation with increasing latitude and in an area phenogram in which populations are progressively nested from south (ancestral) to north (descendant) along the Baja peninsula. Although the geographic concordance of phylogenetic topologies suggests that ancient vicariance events, and not dispersal, have primarily influenced the biogeographic distributions of Bajas vertebrate biota, the phylogeographic structure of L. schottii suggests that Sonoran Desert plant species may exhibit genetic signatures of postglacial range expansion and gene flow as well as vicariance.

Understanding the population genetic structure of Gleditsia triacanthos L.: seed dispersal and variation in female reproductive success

Fine‐scale genetic structuring is influenced by a variety of ecological factors and can directly affect the evolutionary dynamics of plant populations by influencing effective population size and patterns of viability selection. In many plant species, genetic structuring within populations may result from highly localized patterns of seed dispersal around maternal plants or by the correlated dispersal and recruitment of siblings from the same fruit. This fine‐scale genetic structuring may be enhanced if female parents vary significantly in their reproductive success. To test these hypotheses, we used genetic data from 17 allozyme loci and a maximum‐likelihood, ‘maternity‐analysis’ model to estimate individual female fertilities for maternal trees across a large number of naturally established seedlings and saplings in two populations of Gleditsia triacanthos L. (Leguminosae). Maximum‐likelihood fertility estimates showed that the three highest fertility females accounted for 58% of the 313 progeny at the first site and 46% of the 651 progeny at the second site, whereas 18 of 35 and 16 of 34 females, respectively, had fertility estimates that did not exceed 1%. Additional analyses of the second site found individual female fertility to vary significantly both within and among juvenile age classes. Female fertility at the first site was weakly correlated with maternal tree size and spatial location relative to the open, old‐field portions of the population, where the great majority of seedlings and saplings were growing, but no such correlations were found at the second site. Estimates of realized seed dispersal distances indicated that dispersal was highly localized at the first site, but was nearly random at the second site, possibly reflecting differences between the two sites in the behaviour of animal dispersers. The combined estimates of seed dispersal patterns and fertility variation are sufficient to explain previously described patterns of significant fine‐scale spatial genetic structure in these two populations. In general, our results demonstrate that effective seed dispersal distributions may vary significantly from population to population of a species due to the unpredictable behaviour of secondary dispersers. Consequently, the effects of seed dispersal on realized fine‐scale genetic structure may also be relatively unpredictable.

Cascading host-associated genetic differentiation in parasitoids of phytophagous insects

The extraordinary diversity of phytophagous insects may be attributable to their narrow specialization as parasites of plants, with selective tradeoffs associated with alternate host plants driving genetic divergence of host-associated forms via ecological speciation. Most phytophagous insects in turn are attacked by parasitoid insects, which are similarly specialized and may also undergo host-associated differentiation (HAD). A particularly interesting possibility is that HAD by phytophagous insects might lead to HAD in parasitoids, as parasitoids evolve divergent lineages on the new host plant-specific lineages of their phytophagous hosts. We call this process ‘cascading host-associated differentiation’ (cascading HAD). We tested for cascading HAD in parasitoids of two phytophagous insects, each of which consists of genetically distinct host-associated lineages on the same pair of goldenrods (Solidago). Each parasitoid exhibited significant host-associated genetic divergence, and the distribution and patterns of divergence are consistent with divergence in sympatry. Although evidence for cascading HAD is currently limited, our results suggest that it could play an important role in the diversification of parasitoids attacking phytophagous insects. The existence of cryptic host-associated lineages also suggests that the diversity of parasitoids may be vastly underestimated.

THE EVOLUTION OF CALIFORNIA'S WILD RADISH HAS RESULTED IN THE EXTINCTION OF ITS PROGENITORS

Abstract If two previously isolated taxa mutually assimilate through hybridization and subsequent biparental introgression, and if their introgressed descendants have the same or higher fitness than their parents, then gene flow should result in the local extinction of parental taxa via replacement by hybrid derivatives. These dramatic events may occur rapidly, even in a few generations. Given the speed at which such extinction by hybridization may occur, it may be difficult to identify that the process has occurred. Thus, documented instances of extinction by hybridization are rare, and especially so for cases in which both parents are replaced by the hybrid lineage. Here we report morphological and allozyme evidence for the local extinction of two Raphanus species in California via replacement by their hybridderived descendants. The results from a greenhouse experiment demonstrate that California wild radishes have a specific combination of traits from their progenitors, and comparison of our results to that of an earlier report indicate that pure parental types are no longer present in the wild. Our results also show the hybrid‐derived lineage has transgressive fruit weight compared to its parents. Allozyme analysis demonstrates that California wild radishes are derived from hybridization between the putative parental species. However, that analysis also demonstrates that California wild radish has now become an evolutionary entity separate from both of its parents. We suggest that the aggressive colonizing behavior of the hybrid‐derived lineage probably results from a novel combination of parental traits, rather than genetic variability of the population per se.