Lorne M. Wolfe

The evolution of an invasive plant: An experimental study with silene Latifolia

The damage caused by biological invasions has traditionally been thought to result from alien species taking advantage of ecological differences between the native and introduced ranges. In contrast, the role of evolutionary forces has received relatively little attention. Our results show that evolutionary change in Silene latifolia, a North Amer- ican weed that was introduced from Europe about 200 years ago, can help explain the plants successful North American invasion. By growing plants from seed collected in 40 populations from Europe and North America under common garden greenhouse and field conditions, we found significant genetic differences in life history, reproductive, and de- fensive characters. In general, morphological traits and competitive ability remained un- changed, while North American plants germinated earlier, grew faster, produced more flow- ers, had greater survival, and invested less into defensive traits (trichomes, fruit capsule) than their European conspecifics. We suggest that as S. latifolia escaped a suite of specialist enemies, natural selection favored individuals that invest more in growth and reproduction and less in defense.

Population admixture, biological invasions and the balance between local adaptation and inbreeding depression

When previously isolated populations meet and mix, the resulting admixed population can benefit from several genetic advantages, including increased genetic variation, the creation of novel genotypes and the masking of deleterious mutations. These admixture benefits are thought to play an important role in biological invasions. In contrast, populations in their native range often remain differentiated and frequently suffer from inbreeding depression owing to isolation. While the advantages of admixture are evident for introduced populations that experienced recent bottlenecks or that face novel selection pressures, it is less obvious why native range populations do not similarly benefit from admixture. Here we argue that a temporary loss of local adaptation in recent invaders fundamentally alters the fitness consequences of admixture. In native populations, selection against dilution of the locally adapted gene pool inhibits unconstrained admixture and reinforces population isolation, with some level of inbreeding depression as an expected consequence. We show that admixture is selected against despite significant inbreeding depression because the benefits of local adaptation are greater than the cost of inbreeding. In contrast, introduced populations that have not yet established a pattern of local adaptation can freely reap the benefits of admixture. There can be strong selection for admixture because it instantly lifts the inbreeding depression that had built up in isolated parental populations. Recent work in Silene suggests that reduced inbreeding depression associated with post-introduction admixture may contribute to enhanced fitness of invasive populations. We hypothesize that in locally adapted populations, the benefits of local adaptation are balanced against an inbreeding cost that could develop in part owing to the isolating effect of local adaptation itself. The inbreeding cost can be revealed in admixing populations during recent invasions.

Adaptation and colonization history affect the evolution of clines in two introduced species

Phenotypic and genetic clines have long been synonymous with adaptive evolution. However, other processes (for example, migration, range expansion, invasion) may generate clines in traits or loci across geographical and environmental gradients. It is therefore important to distinguish between clines that represent adaptive evolution and those that result from selectively neutral demographic or genetic processes. We tested for the differentiation of phenotypic traits along environmental gradients using two species in the genus Silene, whilst statistically controlling for colonization history and founder effects. We sampled seed families from across the native and introduced ranges, genotyped individuals and estimated phenotypic differentiation in replicated common gardens. The results suggest that post-glacial expansion of S. vulgaris and S. latifolia involved both neutral and adaptive genetic differentiation (clines) of life history traits along major axes of environmental variation in Europe and North America. Phenotypic clines generally persisted when tested against the neutral expectation, although some clines disappeared (and one cline emerged) when the effects of genetic ancestry were statistically removed. Colonization history, estimated using genetic markers, is a useful null model for tests of adaptive trait divergence, especially during range expansion and invasion when selection and gene flow may not have reached equilibrium.

REDUCING ENVIRONMENTAL BIAS WHEN MEASURING NATURAL SELECTION

Abstract.— Crucial to understanding the process of natural selection is characterizing phenotypic selection. Measures of phenotypic selection can be biased by environmental variation among individuals that causes a spurious correlation between a trait and fitness. One solution is analyzing genotypic data, rather than phenotypic data. Genotypic data, however, are difficult to gather, can be gathered from few species, and typically have low statistical power. Environmental correlations may act through traits other than through fitness itself. A path analytic framework, which includes measures of such traits, may reduce environmental bias in estimates of selection coefficients. We tested the efficacy of path analysis to reduce bias by re‐analyzing three experiments where both phenotypic and genotypic data were available. All three consisted of plant species (Impatiens capensis, Arabidopsis thaliana, and Raphanus sativus) grown in experimental plots or the greenhouse. We found that selection coefficients estimated by path analysis using phenotypic data were highly correlated with those based on genotypic data with little systematic bias in estimating the strength of selection. Although not a panacea, using path analysis can substantially reduce environmental biases in estimates of selection coefficients. Such confidence in phenotypic selection estimates is critical for progress in the study of natural selection.

Do floral herbivores respond to variation in flower characteristics in Gelsemium sempervirens (Loganiaceae), a distylous vine?

We tested the hypothesis that traits traditionally thought to function in pollination can also influence attack by floral herbivores. Because distylous species produce two different flower types, we used Gelsemium sempervirens, a distylous vine of southeastern USA, to examine the frequency and pattern of floral herbivory in relation to floral characteristics. Flowers of the short-styled morph had larger corollas but showed no difference in the volume or concentration of nectar produced. Over the 2 yr of this study, 20-30% of plants suffered floral herbivory. The pattern of damage was morph-specific. Long-styled flowers were more likely to have damaged pistils, while stamens were more often damaged in short-styled flowers. In this distylous species, exserted flower organs were more likely to be eaten. Such differential herbivory based on the position of floral organs within a flower may result in reduced fitness via either male (short-styled morph) or female function (long-styled morph).

Does intraspecific hybridization contribute to the evolution of invasiveness?: an experimental test.

One of the major objectives of research on invasive species is to determine the relative importance of different evolutionary and ecological forces in the invasion process. It was recently suggested that post-introduction intraspecific hybridization between previously isolated genotypes could produce novel and/or heterotic progeny that might express enhanced invasiveness. We tested this hypothesis with Silene latifolia, a European native that has successfully invaded North America and has previously been shown to have undergone genetic change since its introduction. In a common garden experiment we compared the performance of plants derived from within and between population crosses from eight European and 18 North American populations. Results showed that there was no significant effect of crossing distance on progeny phenotype. Furthermore, progeny from within or between population crosses did not differ in size, reproductive output or survival. Collectively, these results suggest that the invasive phenotype of S. latifolia is likely the result of natural selection and/or genetic drift rather than intraspecific hybridization.

Do Pollination Syndromes Partition the Pollinator Community? A Test Using Four Sympatric Morning Glory Species

We adopted a comparative approach to evaluate whether pollination (floral) syndromes serve to partition the pollinator fauna among four coflowering species of morning glories (Ipomoea, Convolvulaceae). Two of the species (I. hederacea and I. trichocarpa) fit the “bee” syndrome: they produce blue and purple flowers that have large corolla openings, and they secrete smaller volumes of concentrated nectar. The other two (I. quamoclit and I. hederifolia) exhibit the “bird” syndrome: they have reddish flowers and narrow, tubular corollas, and they secrete larger volumes of dilute nectar. The pollinator fauna of 11 species of lepidoptera, bees, and hummingbird did not visit Ipomoea species in proportion to their relative abundance. The bumblebees foraged exclusively on the blue‐flowered I. hederacea and I. trichocarpa, and the hummingbirds visited only the red‐flowered I. hederifolia and I. quamoclit, while the lepidopterans exhibited less preference for a specific syndrome type. As a group, the Ipomoea species tended to be quite specialized in their use of pollinators. Ca. 75% of the visits to the blue‐flowered I. hederacea and I. trichocarpa were by bumblebees, while ca. 80% of visits to I. quamoclit and I. hederifolia were by sulfur butterflies. Our results support the notion that pollination syndromes do aid in partitioning the pollinator fauna.

Patterns of Phenotypic Plasticity and Their Fitness Consequences in Wild Radish (Raphanus sativus: Brassicaceae)

Phenotypic plasticity, whereby the phenotype expressed by a genotype depends on the environment in which it is raised, may represent two distinct phenomena. First, plastic responses to the environment may be the adaptive outcome of natural selection having favored genotypes that increase their individual fitness by altering their phenotype in response to one or more environmental cues. Second, phenotypic plasticity may simply represent a genotype’s inability to maintain a high‐fitness phenotype under certain environmental conditions (e.g., abiotic stress or limited resources). To determine which of these phenomena characterize the annual plant Raphanus sativus L. (wild radish: Brassicaceae), we conducted a common garden experiment. We examined 19 greenhouse‐bred paternal sibships raised at three planting densities to detect genetic sources of phenotypic variation and to quantify each sibship’s phenotypic plasticity with respect to life‐history traits, floral traits, and fitness components. To determine whether plasticity affected fitness under high‐ and low‐density conditions, we examined the correlation among sibship means between phenotypic plasticity in each measured trait (estimated as the difference between the phenotypic values of the trait in each density) and estimates of fitness in each density. At low density, sibships with the highest plasticity exhibited the highest fitness. In high‐density conditions, no correlation was detected. This indicates that, in wild radish populations where density varies in time or space, highly canalized genotypes are simply those that cannot respond opportunistically to conditions of high resource availability. By contrast, plastic genotypes responded to low density by growing larger and exhibiting higher fitness. We also estimated the “environmental sensitivity” of each paternal sibship and trait as the coefficient of variation of trait means across densities. Traits expressed by individual flowers and fruits (petal size, gynoecium length, pollen and ovule production, pollen size, mean individual seed mass, fruit set, and seed number per fruit) were less sensitive to density than traits more closely related to reproductive output (e.g., lifetime flower production, maternal fecundity), indicating that the former had experienced selection favoring canalized genotypes as phenotypic plasticity in the latter evolved.

A rare continual flowering strategy and its influence on offspring quality in a gynodioecious plant.

The majority of angiosperms have a single annual bout of reproduction; species that flower continually throughout the year are rare. Ochradenus baccatus is a gynodioecious, desert shrub whose principal flowering period is associated with the winter rains, although large individuals also remain in flower during the hot, dry summer. The goal of this study was to examine the reproductive consequences of continual flowering in a large population of O. baccatus in Israel. Over the two years of this study, 60% of individuals flowered continuously. The number of fruit and seeds per fruit were greater in winter. Winter seeds were ∼12% heavier than summer seeds and had significantly higher germination rates (80 vs. 60%, respectively). Although summer seeds were smaller and less likely to germinate, we propose that the benefit derived from their production lies in their ability to capitalize on the first winter rains. These early rain events provide a head start on establishment and growth in the hostile desert environment. Plants that delay reproduction until the onset of rains risk having their offspring face the dry conditions of spring and summer.

REGULATION OF GENDER AND FLOWERING BEHAVIOR IN A SEXUALLY DIMORPHIC DESERT SHRUB (OCHRADENUS BACCATUSDELILE [RESEDACEAE])

The major goal of this study was to examine patterns of gender variation in Ochradenus baccatus , a shrub found in the Judean Desert and Arava Valley of Israel, whose breeding system was previously considered dioecious (separate male and female individuals). We conducted detailed measurements on 150 marked plants over two years to (1) quantitatively describe the variation in sex expression and elucidate the factors responsible for gender variation in males, (2) determine the role of plant size in regulating the flowering behavior through the year, and (3) document pollinator visitation to males and females. The variability in sex expression differed between males and females. Females only reproduced by seed. In contrast, gender in males was extremely variable: 35% of males reproduced only by pollen donation (pure males) and 65% produced pollen and varying amounts of fruit and seeds (inconstant males). The ability to produce fruit was highly correlated with individual plant size. Inconstant males were significantly larger than pure males. Individual plant size also determined the flowering pattern through the year. Unlike most other desert plant species that typically flower after the winter rains, large O. baccatus plants flowered all year. Small plants, regardless of sex, flowered only during the winter months. The flowers of O. baccatus were visited by a diverse suite of insects including wasps, bees, ants, beetles, flies, and butterflies. Perhaps owing to the greater attractiveness of the floral display of males (due to the presence of yellow pollen), males were visited by many more insects than females. Over four observation days, 526 insects were counted on male plants compared to only 39 on females.