Christopher G. Eckert

Genetic variation across species' geographical ranges: the central-marginal hypothesis and beyond

There is growing interest in quantifying genetic population structure across the geographical ranges of species to understand why species might exhibit stable range limits and to assess the conservation value of peripheral populations. However, many assertions regarding peripheral populations rest on the long‐standing but poorly tested supposition that peripheral populations exhibit low genetic diversity and greater genetic differentiation as a consequence of smaller effective population size and greater geographical isolation relative to geographically central populations. We reviewed 134 studies representing 115 species that tested for declines in within‐population genetic diversity and/or increases in among‐population differentiation towards range margins using nuclear molecular genetic markers. On average, 64.2% of studies detected the expected decline in diversity, 70.2% of those that tested for it showed increased differentiation and there was a positive association between these trends. In most cases, however, the difference in genetic diversity between central and peripheral population was not large. Although these results were consistent across plants and animals, strong taxonomic and biogeographical biases in the available studies call for a cautious generalization of these results. Despite the large number of studies testing these simple predictions, very few attempted to test possible mechanisms causing reduced peripheral diversity or increased differentiation. Almost no study incorporated a phylogeographical framework to evaluate historical influences on contemporary genetic patterns. Finally, there has been little effort to test whether these geographical trends in putatively neutral variation at marker loci are reflected by quantitative genetic trait variation, which is likely to influence the adaptive potential of populations across the geographical range.

Plant mating systems in a changing world

There is increasing evidence that human disturbance can negatively impact plant-pollinator interactions such as outcross pollination. We present a meta-analysis of 22 studies involving 27 plant species showing a significant reduction in the proportion of seeds outcrossed in response to anthropogenic habitat modifications. We discuss the evolutionary consequences of disturbance on plant mating systems, and in particular whether reproductive assurance through selfing effectively compensates for reduced outcrossing. The extent to which disturbance reduces pollinator versus mate availability could generate diverse selective forces on reproductive traits. Investigating how anthropogenic change influences plant mating will lead to new opportunities for better understanding of how mating systems evolve, as well as of the ecological and evolutionary consequences of human activities and how to mitigate them.

Evolutionary processes in aquatic plant populations

Abstract Aquatic plants exhibit striking taxonomic, morphological and ecological diversity. This variation limits the ability to pose general hypotheses with regards to evolutionary processes in aquatic plants. Here we ask whether the population structure, reproductive systems, gene flow and patterns of genetic differentiation in aquatic plants are likely to differ in any significant way from terrestrial plants. Defining the limits of aquatic plant populations is best attempted using demographic and genetic techniques for estimating effective population size (Ne. Data available for terrestrial species suggest that Ne in many annual aquatics is likely to be small, a fraction of the census number. In highly clonal species, especially those with water-dispersed vegetative fragments, effective population sizes may differ widely from those of related terrestrial taxa. However, measuring Ne in such species will probably require approaches more similar to those used to study vagile parthenogenetic animals than those used in plant populations. Reproductive systems in aquatic plants, though well described, have only begun to receive quantitative study. Levels of inbreeding and other mating-system parameters have been measured in several emergent species but are lacking for floating-leaved, submerged or free-floating taxa. Extensive clonal propagation presents analytical difficulties but also provides experimental opportunities for studying mating-system variation, particularly the relationship between large clone size and self-fertilization. Limited sexual reproduction has been observed in many highly clonal, aquatic species; there has been little attempt, however, to investigate the extent to which sterility can be attributed to genetic and environmental factors, or to explore whether sterility accumulates in clonal lineages. Gene flow in aquatic plants may be greatly affected by the discrete and patchy nature of many aquatic habitats and the directional transport of propagules in running waters. While the extent of gene movement may be influenced by habitat structure, genetic consequences of local and long-distance dispersal are likely to depend on the type of propagule involved. Transport of vegetative fragments may lead more frequently to successful gene establishment than dispersal of seed, and may, in part, explain the extensive geographical ranges of many clonal aquatic species. A survey of electrophoretic variation in 81 aquatic taxa revealed that the distribution of genetic diversity within and among populations of emergent species, as in their terrestrial counterparts, appears to be determined primarily by their breeding systems and life histories. In contrast, data for several submerged groups suggest widespread genetic monomorphism. The data, however, are limited, making interpretation of this pattern difficult, especially in cases where uniformity at isozyme loci appears to be associated with morphological and physiological differentiation. Further microevolutionary studies of aquatic plant populations may help to clarify the apparent conservative macroevolutionary pattern exhibited by certain aquatic plant families.

Genetic cost of reproductive assurance in a self-fertilizing plant

The transition from outcrossing to self-fertilization is one of the most common evolutionary trends in plants. Reproductive assurance, where self-fertilization ensures seed production when pollinators and/or potential mates are scarce, is the most long-standing and most widely accepted explanation for the evolution of selfing, but there have been few experimental tests of this hypothesis. Moreover, many apparently adaptive floral mechanisms that ensure the autonomous production of selfed seed might use ovules that would have otherwise been outcrossed. This seed discounting is costly if selfed offspring are less viable than their outcrossed counterparts, as often happens. The fertility benefit of reproductive assurance has never been examined in the light of seed discounting. Here we combine experimental measures of reproductive assurance with marker-gene estimates of self-fertilization, seed discounting and inbreeding depression to show that, during 2 years in 10 Ontario populations of Aquilegia canadensis (Ranunculaceae), reproductive assurance through self-fertilization increases seed production, but this benefit is greatly outweighed by severe seed discounting and inbreeding depression.

Plant reproductive systems and evolution during biological invasion

Recent biological invasions provide opportunities to investigate microevolution during contemporary timescales. The tempo and scope of local adaptation will be determined by the intensity of natural selection and the amounts and kinds of genetic variation within populations. In flowering plants, genetic diversity is strongly affected by interactions between reproductive systems and stochastic forces associated with immigration history and range expansion. Here, we explore the significance of reproductive system diversity for contemporary evolution during plant invasion. We focus in particular on how reproductive modes influence the genetic consequences of long‐distance colonization and determine the likelihood of adaptive responses during invasion. In many clonal invaders, strong founder effects and restrictions on sexual reproduction limit opportunities for local adaptation. In contrast, adaptive changes to life‐history traits should be a general expectation in both outbreeding and inbreeding species. We provide evidence that evolutionary modifications to reproductive systems promote the colonizing ability of invading populations and that reproductive timing is an important target of selection during range expansion. Knowledge of the likelihood and speed at which local adaptation evolves in invasive plants will be particularly important for management practices when evolutionary changes enhance ecological opportunities and invasive spread.

CONTRIBUTIONS OF AUTOGAMY AND GEITONOGAMY TO SELF-FERTILIZATION IN A MASS-FLOWERING, CLONAL PLANT

The fitness consequences of self-fertilization are largely determined by how self-pollination occurs. Within-flower self-pollination (autogamy) may be advantageous, since it can provide reproductive assurance without much seed or pollen discounting. In contrast, between-flower self-pollination (geitonogamy) provides no reproductive assurance and can cause severe seed and pollen discounting. I used floral emasculations with marker- gene analysis to estimate the components of self-fertilization in a tristylous, self-compatible, clonal, mass-flowering plant, Decodon verticillatus. This species produces 30% of progeny through selfing. I assessed the contribution of autogamy to selfing by comparing pollen deposition, seed production, and the selfing rate of flowers emasculated before anther dehiscence with intact flowers. Emasculation had no effect on pollen deposition, caused a small increase in seed production, and only reduced self-fertilization by 14%, suggesting that most selfing occurs through geitonogamy. Geitonogamy can be due to self-pollination between flowers on the same branch, different flowering branches of the same plant, or different ramets of the same clonal genet. I assessed the contribution of within-branch geitonogamy by emasculating all flowers on a branch, which reduced selfing from 0.29 + 0.03 (mean ? 1 SE) to 0.19 ? 0.04. Between-branch geitonogamy was estimated by com- paring the selfing rate of plants with only a single flowering branch (0.16 + 0.07) to plants with multiple flowering branches (0.27 ? 0.04). Selfing rates of individual branches also correlated positively with the daily number of flowers open on nonfocal branches of the same plant. Between-ramet geitonogamy was suggested by significant self-fertilization by single-branch plants, even when all flowers were emasculated (0.10 ? 0.07). Selfing rates of individual branches also correlated negatively with measures of local clonal diversity. Based on these results, autogamy accounts for only 18 + 14% of self-fertilization, with the remainder (82 + 17%) due to geitonogamy, which occurs about equally through pol- lination within branches (31 ? 22%), between branches (38 ? 32%), and between ramets (31 ? 28%). Because selfing occurs mostly through geitonogamy and is associated with strong inbreeding depression, it seems disadvantageous. Selfing in D. verticillatus has probably not been selected directly, but is a by-product of self-compatibility, large plant size, mass-flowering, and clonal propagation.

INBREEDING DEPRESSION IN PARTIALLY SELF-FERTILIZING DECODON VERTICILLATUS (LYTHRACEAE): POPULATION-GENETIC AND EXPERIMENTAL ANALYSES

Inbreeding depression is a major selective force favoring outcrossing in flowering plants. Some self‐fertilization, however, should weaken the harmful effects of inbreeding by exposing genetic load to selection. This study examines the maintenance of inbreeding depression in partially self‐fertilizing populations of the long‐lived, herbaceous wetland plant, Decodon verticillatus (L.) Ell. (Lythraceae). Estimates from ten populations indicate that 30% of offspring are produced through self‐fertilization. Population‐genetic estimates of inbreeding depression (δ = 1 – relative mean fitness of selfed progeny) based on changes in the inbreeding coefficient for the same ten populations were uniformly high, ranging from 0.49 to 1.79 and averaging 1.11 ± 0.29 SE. Although confidence intervals of individual population estimates were large, estimates were significantly greater than 0 in six populations and greater than 0.5 in four. Inbreeding depression was also estimated by comparing growth, survival, and flowering of experimentally selfed and outcrossed offspring from two of these populations in a 1‐yr glasshouse experiment involving three density regimes; after which offspring were transplanted into garden arrays and two field sites and monitored for two consecutive growing seasons. Overall δ^ for survival averaged 0.27 ± 0.01 in the glasshouse, 0.33 ± 0.04 in the garden, and 0.46 ± 0.04 in the field. The glasshouse experiment also revealed strong inbreeding depression for growth variables, especially above‐soil dry weight ( δ^ = 0.42 ± 0.03). The fitness consequences of inbreeding depression for these growth variables approximately doubles if survival to maturity is determined by severe truncation selection. Despite substantial selfing, inbreeding depression appears to be a major selective force favoring the maintenance of outcrossing in D. verticillatus.

Evolutionary constraints on adaptive evolution during range expansion in an invasive plant

Biological invasions may expose populations to strong selection for local adaptation along geographical gradients in climate. However, evolution during contemporary timescales can be constrained by low standing genetic variation and genetic correlations among life-history traits. We examined limits to local adaptation associated with northern migration of the invasive wetland plant purple loosestrife (Lythrum salicaria) using a selection model incorporating a trade-off between flowering time and size at reproduction, and common garden experiments of populations sampled along a latitudinal transect of approximately 1200 km in eastern North America. A strong trade-off between flowering time and size at reproduction caused early-flowering plants to be smaller with reduced seed production in northern populations. Northward spread was associated with a decline in genetic variance within populations and an increase in genetic skew for flowering time and size, with limited genetic variation for small, early-flowering genotypes. These patterns were predicted by our selection model of local adaptation to shorter growing seasons and were not consistent with expectations from non-adaptive processes. Reduced fecundity may limit population growth and rates of spread in northern populations. Identifying genetic constraints on key life-history traits can provide novel insights into invasion dynamics and the causes of range limits in introduced species.

Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation

Reduced allocation to structures for pollinator attraction is predicted in selfing species. We explored the association between outcrossing and floral display in a broad sample of angiosperms. We used the demonstrated relationship to test for bias against selfing species in the outcrossing rate distribution, the shape of which has relevance for the stability of mixed mating. Relationships between outcrossing rate, flower size, flower number and floral display, measured as the product of flower size and number, were examined using phylogenetically independent contrasts. The distribution of floral displays among species in the outcrossing rate database was compared with that of a random sample of the same flora. The outcrossing rate was positively associated with the product of flower size and number; individually, components of display were less strongly related to outcrossing. Compared with a random sample, species in the outcrossing rate database showed a deficit of small floral display sizes. We found broad support for reduced allocation to attraction in selfing species. We suggest that covariation between mating systems and total allocation to attraction can explain the deviation from expected trade-offs between flower size and number. Our results suggest a bias against estimating outcrossing rates in the lower half of the distribution, but not specifically against highly selfing species.

Re‐establishment of clinal variation in flowering time among introduced populations of purple loosestrife (Lythrum salicaria, Lythraceae)

Range expansion during biological invasion requires that invaders adapt to geographical variation in climate, which should yield latitudinal clines in reproductive phenology. We investigated geographic variation in life history among 25 introduced populations of Lythrum salicaria, a widespread European invader of North American wetlands. We detected a strong latitudinal cline in initiation of flowering and size at flowering, which paralleled that reported among native populations. Plants from higher latitudes flowered earlier and at a smaller size than those from lower latitudes, even when raised in a uniform glasshouse. Early flowering was associated with greatly reduced reproductive output, but this was not associated with latitudinal variation in abundance, and probably did not result from a genetic correlation between time to and size at flowering. As introduction to North America c. 200 years ago, L. salicaria has re‐established latitudinal clines in life history, probably as an evolutionary response to climatic selection.