Rachel B. Spigler

In a long-term experimental demography study, excluding ungulates reversed invader's explosive population growth rate and restored natives

Significance In ecosystems worldwide, the presence of overabundant ungulates (e.g. deer, cows) and the invasion of exotic plants are disrupting native communities. A recent hypothesis causally links these problems implicating overabundant ungulates in enhancing invaders’ demographic success. We tested this hypothesis in a forest where white-tailed deer are overabundant and garlic mustard is aggressively invading. Using long-term, replicated deer exclusion/deer access plot pairs, we quantified population density, growth, and decline of this invader and native plants. We conclusively demonstrate that deer are required for garlic mustard success; its local extinction is projected where deer are absent. Our findings provide the first definitive support connecting overabundant ungulates to enhanced invader success, with broad implications for biodiversity and ecosystem function. A major goal in ecology is to understand mechanisms that increase invasion success of exotic species. A recent hypothesis implicates altered species interactions resulting from ungulate herbivore overabundance as a key cause of exotic plant domination. To test this hypothesis, we maintained an experimental demography deer exclusion study for 6 y in a forest where the native ungulate Odocoileus virginianus (white-tailed deer) is overabundant and Alliaria petiolata (garlic mustard) is aggressively invading. Because population growth is multiplicative across time, we introduce metrics that correctly integrate experimental effects across treatment years, the cumulative population growth rate, λc, and its geometric mean, λper-year, the time-averaged annual population growth rate. We determined λc and λper-year of the invader and of a common native, Trillium erectum. Our results conclusively demonstrate that deer are required for the success of Alliaria; its projected population trajectory shifted from explosive growth in the presence of deer (λper-year = 1.33) to decline toward extinction where deer are excluded (λper-year = 0.88). In contrast, Trillium’s λper-year was suppressed in the presence of deer relative to deer exclusion (λper-year = 1.04 vs. 1.20, respectively). Retrospective sensitivity analyses revealed that the largest negative effect of deer exclusion on Alliaria came from rosette transitions, whereas the largest positive effect on Trillium came from reproductive transitions. Deer exclusion lowered Alliaria density while increasing Trillium density. Our results provide definitive experimental support that interactions with overabundant ungulates enhance demographic success of invaders and depress natives’ success, with broad implications for biodiversity and ecosystem function worldwide.

Comparative Genetic Mapping Points to Different Sex Chromosomes in Sibling Species of Wild Strawberry (Fragaria)

Separate sexes have evolved repeatedly from hermaphroditic ancestors in flowering plants, and thus select taxa can provide unparalleled insight into the evolutionary dynamics of sex chromosomes that are thought to be shared by plants and animals alike. Here we ask whether two octoploid sibling species of wild strawberry—one almost exclusively dioecious (males and females), Fragaria chiloensis, and one subdioecious (males, females, and hermaphrodites), F. virginiana—share the same sex-determining chromosome. We created a genetic map of the sex chromosome and its homeologs in F. chiloensis and assessed macrosynteny between it and published maps of the proto-sex chromosome of F. virginiana and the homeologous autosome of hermaphroditic diploid species. Segregation of male and female function in our F. chiloensis mapping population confirmed that linkage and dominance relations are similar to those in F. virginiana. However, identification of the molecular markers most tightly linked to the sex-determining locus in the two octoploid species shows that, in both, this region maps to homeologues of chromosome 6 in diploid congeners, but is located at opposite ends of their respective chromosomes.

GENETIC ARCHITECTURE OF SEXUAL DIMORPHISM IN A SUBDIOECIOUS PLANT WITH A PROTO‐SEX CHROMOSOME

The rise of sexual dimorphism is thought to coincide with the evolution of sex chromosomes. Yet because sex chromosomes in many species are ancient, we lack empirical evidence of the earliest stages of this transition. We use QTL analysis to examine the genetic architecture of sexual dimorphism in subdioecious octoploid Fragaria virginiana. We demonstrate that the region housing the male‐function locus controls the majority of quantitative variation in proportion fruit set, confirming the existence of a proto‐sex chromosome, and houses major QTL for eight additional sexually dimorphic traits, consistent with theory and data from animals and plants with more advanced sex chromosomes. We also detected autosomal QTL, demonstrating contributions to phenotypic variation in sexually dimorphic traits outside the sex‐determining region. Moreover, for proportion seed set we found significant epistatic interactions between autosomal QTL and the male‐function locus, indicating sex‐limited QTL. We identified linked QTL reflecting trade‐offs between male and female traits expected from theory and positive integration of male traits. These findings indicate the potential for the evolution of greater sexual dimorphism. Involvement of linkage groups homeologous to the proto‐sex chromosome in these correlations reflects the polyploid origin of F. virginiana and raises the possibility that chromosomes in this homeologous group were predisposed to become the sex chromosome.

Sex ratio and subdioecy in Fragaria virginiana: the roles of plasticity and gene flow examined

Here we examined the roles of sex-differential plasticity (SDP) and gene flow in sex ratio evolution of subdioecious Fragaria virginiana. We assessed whether female frequency varied with resource availability in 17 natural populations and then characterized plasticity and mean investment in allocation to female function at flower and plant levels in the sex morphs in the glasshouse. We estimated patterns of population divergence using five microsatellite markers. We reveal SDP in fruit production substantial enough to translate into a higher equilibrium female frequency at low resources. Thus SDP can account, in part, for the strong negative relationship between female frequency and resources found in the field. Pollen-bearing morphs varied in plasticity across populations, and the degree of plasticity in fruit number was positively correlated with in situ variation in nitrogen (N) availability, suggesting an adaptive component to sex-allocation plasticity. Low neutral genetic differentiation, indicating high gene flow or recent divergence, may contribute to the absence of population differentiation in fruit-setting ability of pollen-bearing morphs despite considerable sex ratio variation. We consider how these processes, in addition to other features of this system, may work in concert to influence sex ratios and to hinder the evolution of dioecy in F. virginiana.

Sex-allocation plasticity in hermaphrodites of sexually dimorphic Fragaria virginiana (Rosaceae)

Sex-allocation plasticity is thought to play an important role in the evolution of separate sexes in plants. Accordingly, much attention has been paid to environmentally induced variation in fruit and seed production in sexually dimorphic species, but we know little about whether this variation arises as a direct response to environmental variation or is instead an indirect consequence of changes in plant size. In this study, we characterize sex-allocation plasticity across a resource gradient for several reproductive traits in hermaphrodites of gyno(sub)dioecious Fragaria virginiana Duch. We find significant plasticity, on average, for flower number, proportion fruit set, ovule number, proportion seed set, and runner number in response to resource variation. Plasticity of most traits examined tended to be at least partially independent of variation in plant size, suggesting that it is not simply an indirect consequence of plant allometry. Moreover, we find genetic variation for plasticity of key reproduc...

Context-dependency of resource allocation trade-offs highlights constraints to the evolution of floral longevity in a monocarpic herb

Floral longevity is a critical component of floral display, yet there is a conspicuous paucity of empirical research on its evolution within species. Evolutionary models of floral longevity are grounded in resource allocation theory and propose that selection acts on heritable variation to optimize longevity in light of competing floral construction and maintenance costs. Key assumptions remain untested within wild species. We measured maximum floral longevity alongside protandry, flower size, flower number and flowering rate across families of the monocarpic herb Sabatia angularis grown under high and low resources. We evaluated genetic variation, plasticity and correlations between display traits, including fundamental resource-allocation trade-offs and their interactions with resource availability. All display traits showed significant genetic variation. Resource availability influenced mean floral longevity and flower number, with genetic variation in these responses. Importantly, both floral longevity-flower number and flower number-size trade-offs were significant and stronger under low resources. This study reinforces the application of resource allocation theory to floral display trait evolution. Our work highlights the context-dependency of trade-offs and the potential importance of plasticity in resource allocation, with plants investing in the construction of new flowers at faster rates when resources are high rather than in the maintenance of longer-lived flowers.

Persistent pollinators and the evolution of complete selfing

Th e diversity of plant mating systems has inspired many researchers including Darwin (1876) to ponder why and how these systems have evolved. In particular, mating via a combination of selfi ng and outcrossing (“mixed mating”) has classically been posed as a paradox; models considering the fundamental genetic parameters driving mating-system evolution—the automatic transmission advantage and inbreeding depression—predict evolutionary stability only of complete selfi ng or complete outcrossing. In brief, because selfers and outcrossers both transmit copies of genes through pollen but selfers transmit twice as many through seed, selfers have an automatic advantage at the gene-level compared to outcrossers ( Fig. 1A ). Consequently, selfi ng should fi x in the population unless the relative reduction in fi tness of inbred vs. outbred progeny (inbreeding depression) outweighs the 50% transmission advantage, in which case outcrossing should be fi xed. Yet numerous studies show that species exhibit mixed mating ( Fig. 2 ). Many researchers (including us) have approached studying the evolution of mixed mating by asking, “Why might selfi ng persist despite high inbreeding depression?” ( Fig. 2 , section II). Interestingly, data also show that mixed mating and even high rates of outcrossing (>0.8) are common in self-compatible populations where inbreeding depression is below 0.5 ( Fig. 2 , sections IV and V). Here, we turn the original question around to ask, “Why might outcrossing persist in populations despite relatively low inbreeding depression?” and consider constraints posed by pollinator mutualists. Understanding the evolution of selfing given high inbreeding depression is perhaps best explained considering outcross pollen limitation. Th e reproductive assurance hypothesis posits that unreliable pollinators or low mate availability leave plants no better fi tness option but to self, given the alternative of making fewer or even no seeds. A number of excellent models incorporate outcross pollen limitation ( Goodwillie et al., 2005 ), and empirical studies support components of the reproductive assurance hypothesis ( Busch and Delph, 2012 ). While this hypothesis is well accepted as an important driver of the evolution of selfi ng and the maintenance of mixed mating, it is one-sided in shedding light on mating system evolution because it does not explain moderate to high levels of outcrossing when inbreeding depression is low . We proff er that an explanation for persistent outcrossing given low inbreeding depression may lie in viewing the evolution of selfi ng through the lens of mutualism breakdown ( Sachs and Simms, 2006 ) and the potential difficulties for self-compatible plants in divesting from their mutualist pollinators. Conflict could arise from the evolution of higher autonomous selfing rates because, while autonomously selfi ng plants are less reliant on their pollinator mutualists, there are ecological conditions where pollinators may remain strongly reliant on the plant for pollen and nectar. The resulting asymmetry would effect continued outcross pollen delivery, significantly slowing the progression of mutualism abandonment by the plant and thus evolution to high selfi ng. Notably, the asymmetry should be greatest where pollinators are abundant. Yet, pollen limitation is often seen as ubiquitous. Despite this perception, conditions with abundant pollinators providing adequate outcross pollen may be common. Indeed, Knight et al. (2006) revealed clear publication bias for reporting pollen limitation and that, when measured over a plant’s lifetime, the magnitude of pollen limitation on average is actually low, especially for monocarpic species, which constitute half of the species inhabiting the seemingly paradoxical state space of moderate to high outcrossing levels with low inbreeding ( Fig. 2 , sections IV and V). 1 Manuscript received 21 August 2017; revision accepted 4 October 2017. 2 Department of Biology, Temple University, 1900 N. 12th Street, Philadelphia, Pennsylvania 19122 USA; and 3 Department of Ecology & Evolutionary Biology, Th e University of Tennessee, Knoxville, 569 Dabney Hall, Knoxville, Tennessee 37996 USA 4 Author for correspondence (e-mail: rachel.spigler@temple.edu); ORCID id 0000-00025997-9781 https://doi.org/10.3732/ajb.1700332 O N T H E N AT U R E O F T H I N G S : E S S AY S New Ideas and Directions in Botany