Stuart Wagenius

COMMUNITY GENETICS: EXPANDING THE SYNTHESIS OF ECOLOGY AND GENETICS

Community genetics synthesizes community ecology and population genetics and yields fresh insights into the interplay between evolutionary and ecological processes. A community genetics framework proves especially valuable when strong selection on traits results from or impinges on interspecific interactions, an increasingly common phenomenon as more communities are subject to direct management or anthropogenic disturbances. We draw illustrations of this perspective from our ongoing studies of three representative communities, two managed and one natural, that have recently undergone large perturba- tions. The studied communities are: (1) insect pests of crop plants genetically engineered to produce insecticidal toxins; (2) insect-pollinated plants in habitats severely fragmented by agriculture and urbanization; and (3) a pathogen and its crop host now grown extensively outside their native ranges. We demonstrate the value of integrating genetic and ecological processes to gain a full understanding of community dynamics, particularly in nonequilib- rium systems that are subject to strong selection.

Patch Aging and the S-Allee Effect: Breeding System Effects on the Demographic Response of Plants to Habitat Fragmentation

We used empirical and modeling approaches to examine effects of plant breeding systems on demographic responses to habitat fragmentation. Empirically, we investigated effects of local flowering plant density on pollination and of population size on mate availability in a common, self‐incompatible purple coneflower, Echinacea angustifolia, growing in fragmented prairie habitat. Pollination and recruitment increased with weighted local density around individual flowering plants. This positive density dependence is an Allee effect. In addition, mean mate compatibility between pairs of plants increased with population size. Based on this empirical study, we developed an individual‐based, spatially explicit demographic model that incorporates autosomal loci and an S locus. We simulated habitat fragmentation in populations identical except for their breeding system, self‐incompatible (SI) or self‐compatible (SC). Both populations suffered reduced reproduction in small patches because of scarcity of plants within pollination distance (potential mates) and inbreeding depression. But SI species experienced an additional, genetic contribution to the Allee effect (S‐Allee effect) caused by allele loss at the S locus, which reduces mate availability, thereby decreasing reproduction. The strength of the S‐Allee effect increases through time (i.e., patches age) because random genetic drift reduces S‐allele richness. We investigate how patch aging influences extinction and discuss how the S‐Allee effect influences communities in fragmented habitat.

SCALE DEPENDENCE OF REPRODUCTIVE FAILURE IN FRAGMENTED Echinacea POPULATIONS

I investigated reproduction in a three-year study of Echinacea angustifolia, purple coneflower, growing in a fragmented prairie landscape. I quantified the local abundance of flowering conspecifics at individual-based spatial scales and at a population-based spatial scale. Regression analyses revealed that pollen limitation increased while seed set and fecundity decreased with isolation of individual plants. Isolation, defined as the distance to the k(th) nearest flowering conspecific, was a good predictor of pollen limitation, for all nearest neighbors considered (k = 1-33), but the strength of the relationship, as quantified by R2, peaked at intermediate scales (k = 2-18). The relationship of isolation to seed set and fecundity was similarly strongest at intermediate scales (k = 3-4). The scale dependence of individual density effects on reproduction (density of flowering plants within x meters) resembled that of isolation. Analyses at a population-based scale showed that pollen limitation declined significantly with population size. Seed set and fecundity also declined with population size, but significantly so only in 1998. Whether quantifying local abundance with population- or individual-based measures, reproductive failure due to pollen limitation is a consistent consequence of Echinacea scarcity. However, individual-based measures of local abundance predicted pollen limitation from a wider sample of plants with a simpler model than did population size. Specifically, the largest site, a nature preserve, is composed of plants with intermediate individual isolation and, as predicted, intermediate pollen limitation, but its large population size poorly predicted population mean pollen limitation.

Reproduction of Echinacea angustifolia in fragmented prairie is pollen‐limited but not pollinator‐limited

Pollen limitation of plant reproduction occurs in many plant species, particularly those in fragmented habitat; however, causes of pollen limitation are often unknown. We investigated the relationship between pollen limitation and pollinator visitation in the purple coneflower, Echinacea angustifolia (Asteraceae), which grows in the extremely fragmented tall grass prairie of North America. Previous investigations showed that pollen limitation of E. angustifolia increases with plant isolation and decreases with population size. We observed insect visitation to E. angustifolia over two flowering seasons and estimated pollen limitation of observed plants, using seed set as a proxy measure in 2004 and persistence of receptive style rows in 2005. We analyzed spatial patterns of bee visitation and pollination at two spatial scales: individual isolation, as measured by the distance to their kth nearest flowering neighbors (k = 1 - 15), and population size. Our results indicate that E. angustifolia is pollinated by over 26 species of native bees, with 70-75% of visits by halictid bees. Surprisingly, in both years, bee visitation increased with isolation of individual plants and did not vary significantly with population size. As expected, plant isolation increased pollen limitation and lowered seed set. There was no effect of population size on seed set in 2004, and pollen limitation decreased nonsignificantly with population size in 2005. We conclude that pollen receipt limits reproduction in E. angustifolia, but pollinator visitation does not. Remarkably, isolated plants simultaneously have increased rates of pollinator visitation by pollinators and decreased reproduction. We discuss alternative explanations of pollen limitation that are consistent with this apparent discrepancy, including a decline in the availability of compatible conspecific pollen with increased plant isolation.

Biparental inbreeding and interremnant mating in a perennial prairie plant: Fitness consequences for progeny in their first eight years

Despite fundamental importance to population dynamics, mating system evolution, and conservation management, the fitness consequences of breeding patterns in natural settings are rarely directly and rigorously evaluated. We experimentally crossed Echinacea angustifolia, a widespread, perennial prairie plant undergoing radical changes in distribution and abundance due to habitat fragmentation. We quantified the effects of both biparental inbreeding and crossing between remnant populations on progeny survival and reproduction in the field over the first eight years. Lifetime fitness is notoriously difficult to assess particularly for iteroparous species because of the long sequence and episodic nature of selection events. Even with fitness data in hand, analysis is typically plagued by nonnormal distributions of overall fitness that violate the assumptions of the usual parametric statistical approaches. We applied aster modeling, which integrates the measurements of separate, sequential, nonnormally distributed annual fitness components, and estimated current biparental inbreeding depression at 68% in progeny of sibling‐mating. The effect of between‐remnant crossing on fitness was negligible. Given that relatedness among individuals in remnant populations is already high and dispersal very limited, inbreeding depression may profoundly affect future dynamics and persistence of these populations, as well as their genetic composition.

Style Persistence, Pollen Limitation, and Seed Set in the Common Prairie Plant Echinacea angustifolia (Asteraceae)

Pollen limitation of seed set in flowering plants has important ramifications for the population dynamics, evolution, and conservation of plant populations. I conducted a pollen addition and exclusion experiment demonstrating that style persistence signifies pollen limitation in the narrow‐leaved purple coneflower Echinacea angustifolia, a species native to the North American prairie and plains. I developed a measure of style persistence, SP, a novel way to quantify pollen limitation in individual plants during the flowering season. Using this measure, I investigated the relationship between pollen limitation and seed set over two years in 19 and 27 natural remnant populations in an agricultural landscape. Population mean rates of seed set per plant varied from 0% to 54% in 1997 and from 0% to 63% in 1998. I found that pollen limitation reduced annual reproductive fitness within and among the populations studied. An analysis of the relationship between floret production and the rate of seed set provided no evidence that resource limitation influenced the rate of seed set. I estimated annual fecundity per plant as the product of the rate of seed set per floret, a pollen‐limited process, and floret production per plant, likely a resource‐limited process. Population means of individual annual fecundity ranged from 0 to 182 in 1997 and from 0 to 156 in 1998 and were predicted by population means of SP and the rate of seed set, but not by floret production. The effect of pollen limitation, as quantified by SP, overrides the strong, fundamental relationship between fecundity and floret production. This finding shows that populations consisting of large plants with large floral displays do not necessarily produce more seeds per plant.

Mating between Echinacea angustifolia (Asteraceae) individuals increases with their flowering synchrony and spatial proximity

PREMISE OF THE STUDY Although spatial distance is considered the primary factor in determining plant mating patterns, flowering time and synchrony are also likely to be important. METHODS We quantified the relationships of both distance and flowering phenology to the probability of mating between individual plants. In an experimental plot, we followed daily flowering phenology in Echinacea angustifolia, a self-incompatible perennial pollinated by solitary bees. We assigned paternity to 832 of 927 seedlings from 37 maternal plants using 11 microsatellite loci. Potential pollen donors included the experiment plots 202 flowering plants and a nearby plots 19 flowering plants. For each maternal plant sampled, we examined the pollen pool by quantifying correlated paternity and the effective number of pollen donors. KEY RESULTS Significantly more pollinations occurred between neighboring and synchronous plants than expected under random mating, with distance being more important than flowering synchrony. The distance pollen moved varied over the course of the season, with late flowering plants mating with more distant plants compared to early or peak flowering plants. All maternal plants had a diverse set of mates (mean number of effective pollen donors = 23.7), and the composition of the pollen pools overlapped little between maternal plants. CONCLUSION Both distance and flowering synchrony influenced pollination patterns in E. angustifolia. Our results suggest that pollen movement between incompatible mates and flowering asynchrony could be contributing to the reduced seed set observed in small E. angustifolia remnants. However, we also found that individual plants receive pollen from a diverse group of pollen donors.

The Effect of Plant Inbreeding and Stoichiometry on Interactions with Herbivores in Nature: Echinacea angustifolia and Its Specialist Aphid

Fragmentation of once widespread communities may alter interspecific interactions by changing genetic composition of interacting populations as well as their abundances and spatial distributions. In a long-term study of a fragmented population of Echinacea angustifolia, a perennial plant native to the North American prairie, we investigated influences on its interaction with a specialist aphid and tending ants. We grew plant progeny of sib-matings (I), and of random pairings within (W) and between (B) seven remnants in a common field within 8 km of the source remnants. During the fifth growing season, we determined each plants burden of aphids and ants, as well as its size and foliar elemental composition (C, N, P). We also assayed composition (C, N) of aphids and ants. Early in the season, progeny from genotypic classes B and I were twice as likely to harbor aphids, and in greater abundance, than genotypic class W; aphid loads were inversely related to foliar concentration of P and positively related to leaf N and plant size. At the end of the season, aphid loads were indistinguishable among genotypic classes. Ant abundance tracked aphid abundance throughout the season but showed no direct relationship with plant traits. Through its potential to alter the genotypic composition of remnant populations of Echinacea, fragmentation can increase Echinaceas susceptibility to herbivory by its specialist aphid and, in turn, perturb the abundance and distribution of aphids.

How functional traits, herbivory, and genetic diversity interact in Echinacea: implications for fragmented populations

Habitat fragmentation produces small, spatially isolated populations that promote inbreeding. Remnant populations often contain inbred and outbred individuals, but it is unclear how inbreeding relative to outbreeding affects the expression of functional traits and biotic interactions such as herbivory. We measured a suite of 12 functional traits and herbivore damage on three genotypic cross types in the prairie forb, Echinacea angustifolia: inbred, and outbred crosses resulting from matings within and between remnant populations. Inbreeding significantly affected the expression of all 12 functional traits that influence resource capture. Inbred individuals had consistently lower photosynthetic rates, water use efficiencies, specific leaf areas, and had higher trichome numbers, percent C, and percent N than outbred individuals. However, herbivore damage did not differ significantly among the cross types and was not correlated with other leaf functional traits. Leaf architecture and low physiological rates of the inbred compared to outbred individuals imply poorer capture or use of resources. Inbred plants also had lower survival and fitness relative to outbred plants. Our results show that inbreeding, a phenomenon predicted and observed to occur in fragmented populations, influences key functional traits such as plant structure, physiology and elemental composition. Because of their likely role in fitness of individuals and ecological dynamics plant functional traits can serve as a bridge between evolution and community or ecosystem ecology.

Mating Opportunity Increases with Synchrony of Flowering among Years More than Synchrony within Years in a Nonmasting Perennial

The timing and synchrony of mating activity in a population may vary both within and among years. With the exception of masting species, in which reproductive activity fluctuates dramatically among years, mating synchrony is typically studied within years. However, opportunities to mate also vary among years in nonmasting iteroparous species. We demonstrate that studying only within-year flowering synchrony fails to accurately quantify variation in mating opportunity in an experimental population (n=286) of a nonmasting species, Echinacea angustifolia. We quantified individuals’ synchrony of flowering within and among years and partitioned the contribution of each measure to mean daily mating potential, the number of potential mates per individual per day, averaged over every day that it flowered during the 11-year study period. Individual within- and among-year synchrony displayed wide variation and were weakly correlated. In particular, among-year synchrony explained 39% more variation in mean daily mating potential than did within-year synchrony. Among-year synchrony could have underappreciated significance for mating dynamics in nonmasting species.