Susan Kalisz

The causes of natural selection.

We discuss the necessary and sufficient conditions for identifying the cause of natural selection on a phenotypic trait. We reexamine the observational methods recently proposed for measuring selection in natural populations and illustrate why the multivariate analysis of selection is insufficient for identifying the causal agents of selection. We discuss how the observational approach of multivariate selection analysis can be complemented by experimental manipulations of the phenotypic distribution and the environment to identify not only how selection is operating on the phenotypic distribution but also why it operates in the observed manner. A significant point of departure of our work from recent discussions is in regard to the role of the environment in the study of natural selection. Instead of viewing the environment as a source of unwanted variation that obscures the relationship between phenotype and fitness, we view fitness as arising from the interaction of the phenotype with the environment. The biotic and abiotic environment is the context that gives rise to the relationship between phenotype and fitness (selection). The analysis of the causes of selection is in essence a problem in ecology. The experimental study of the association between selection gradients and environmental characteristics is necessary to identify the agents of natural selection. We recommend research methods for identifying the agency of selection that depend upon a reciprocity between the observational approach of multivariate selection analysis and the manipulative approach of field experiments in evolutionary ecology.

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.

Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating.

The evolution of self-fertilization in hermaphrodites is opposed by costs that decrease the value of self progeny relative to that of outcross progeny. However, self-fertilization is common in plants; 20% are highly selfing and 33% are intermediate between selfing and outcrossing. Darwin proposed an adaptive benefit of self-pollination in providing reproductive assurance when outcrossing is impossible. Moreover, if outcross pollen receipt is inconsistent within or between years, these conditions likewise favour self-pollination, and this can result in a mixture of self and outcross seed production (mixed mating). Despite wide acceptance, the reproductive assurance hypothesis has lacked the support of complete empirical evidence to show that variable pollination can create both the ecological and genetic conditions favouring self-pollination. We recently showed in Collinsia verna that during periods of infrequent pollinator visits, autonomous self-pollination boosted seed output per flower, the key ecological condition. Here we show low inbreeding depression and marker-based estimates of selfing, demonstrating that when the pollination environment in wild populations necessitates reproductive assurance, selfing rates increase. We provide a complete demonstration of reproductive assurance under variable pollination environments and mechanistically link reproductive assurance to intermediate selfing rates through mixed mating.

LONGEVITY CAN BUFFER PLANT AND ANIMAL POPULATIONS AGAINST CHANGING CLIMATIC VARIABILITY

Both means and year-to-year variances of climate variables such as temperature and precipitation are predicted to change. However, the potential impact of changing climatic variability on the fate of populations has been largely unexamined. We analyzed multiyear demographic data for 36 plant and animal species with a broad range of life histories and types of environment to ask how sensitive their long-term stochastic population growth rates are likely to be to changes in the means and standard deviations of vital rates (survival, reproduction, growth) in response to changing climate. We quantified responsiveness using elasticities of the long-term population growth rate predicted by stochastic projection matrix models. Short-lived species (insects and annual plants and algae) are predicted to be more strongly (and negatively) affected by increasing vital rate variability relative to longer-lived species (perennial plants, birds, ungulates). Taxonomic affiliation has little power to explain sensitivity to increasing variability once longevity has been taken into account. Our results highlight the potential vulnerability of short-lived species to an increasingly variable climate, but also suggest that problems associated with short-lived undesirable species (agricultural pests, disease vectors, invasive weedy plants) may be exacerbated in regions where climate variability decreases.

SEX AMONG THE FLOWERS: THE DISTRIBUTION OF PLANT MATING SYSTEMS

Previous reviews of plant outcrossing rate survey data have agreed that predominant selfing and predominant outcrossing are alternative stable states of mating system evolution. We reanalyzed the most recent data and plot outcrossing rates as a continuous variable rather than as a class variable. Wind‐pollinated species are indeed bimodal. However, the shape of the distributions for animal‐pollinated species reveals that intermediate rates of outcrossing are common (49% of species fall between 20% and 80% outcrossing). Consequently, we suggest that mating system is best considered a continuous rather than a discrete character of plant populations.

DEMOGRAPHY OF AN AGE-STRUCTURED ANNUAL: RESAMPLED PROJECTION MATRICES, ELASTICITY ANALYSES, AND SEED BANK EFFECTS'

The role of age—structured seed banks in influencing population dynamic parameters was investigated in a natural population of the winter annual Collinsia verna. Seed persistence was quantified by creating experimental seed banks in the field with seeds of known age. Survival and fecundities of adult plant stages were determined in quadrats of naturally occurring individuals in the field population. Bootstrapping was applied to the resulting data set to estimate means and 95% confidence intervals for population growth rate, stable age distributions, reproductive values, and elasticities. Analyses were performed to determine the extent of variation in these demographic parameters between two consecutive years and between three transects within each year. The results indicate that the presence of a seed bank, even of short duration, was critical to the demography of this population. The population was expanding rapidly in the 1st year of the study (growth rate 1.80), but was declining during the 2nd year (0.41). While the seed bank was demographically important in some transects during the good year (Year 1) the demographic effects of the seed bank were seen most significantly in the poor year (Year 2). The results of this study indicate the need for including age—structured seed banks in demographic analyses and the potential importance of seeds in age—structured seed banks in the shaping of plant life histories.

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.

Evolutionary consequences of self- fertilization in plants

The transition from outcrossing to self-fertilization is one of the most common evolutionary changes in plants, yet only about 10–15% of flowering plants are predominantly selfing. To explain this phenomenon, Stebbins proposed that selfing may be an ‘evolutionary dead end’. According to this hypothesis, transitions from outcrossing to selfing are irreversible, and selfing lineages suffer from an increased risk of extinction owing to a reduced potential for adaptation. Thus, although selfing can be advantageous in the short term, selfing lineages may be mostly short-lived owing to higher extinction rates. Here, we review recent results relevant to the ‘dead-end hypothesis’ of selfing and the maintenance of outcrossing over longer evolutionary time periods. In particular, we highlight recent results regarding diversification rates in self-incompatible and self-compatible taxa, and review evidence regarding the accumulation of deleterious mutations in selfing lineages. We conclude that while some aspects of the hypothesis of selfing as a dead end are supported by theory and empirical results, the evolutionary and ecological mechanisms remain unclear. We highlight the need for more studies on the effects of quantitative changes in outcrossing rates and on the potential for adaptation, particularly in selfing plants. In addition, there is growing evidence that transitions to selfing may themselves be drivers of speciation, and future studies of diversification and speciation should investigate this further.

The mechanism of delayed selfing in Collinsia verna (Scrophulariaceae)

Collinsia verna, blue-eyed Mary, has floral attributes of an outcrossing species, yet most flowers readily self-pollinate under greenhouse conditions. Here we describe the mechanism of self-pollination in C. verna via changes in relative positions of the stigma and anthers and late timing of receptivity, resulting in delayed selfing. Each flower contains four anthers that dehisce sequentially over ∼1 wk. Pollen that is not collected by pollinators accumulates in the keel petal and retains high viability (>80% pollen germination) up to the time of corolla abscission. The stigmatic surface does not become receptive until after the third anther dehisces. This overlap in the sexual phases is concurrent with a change in herkogamy during floral development. In most flowers (70%), the stigma has moved to the front of the keel and is positioned near the anthers when the third anther dehisces. Under field conditions, fruiting success of plants within pollinator exclosures was ∼75% of the fruiting success in open-pollinated plants (33% fruiting success via autogamy vs. 44% fruiting success, respectively). Collinsia verna plants in pollinator exclosures exhibit variation in autogamy rates within natural populations (range 0-80%). In addition, only half of naturally pollinated, receptive flowers examined had pollen tubes growing in their styles. In contrast, shortly after corolla abscission, nearly all flowers examined (96%) had pollen tubes in their styles. Thus we find that in C. verna, autogamy occurs late in floral development, which has the potential to provide substantial reproductive assurance, and that individuals vary in their ability to set fruit through this mechanism. We suggest that delayed selfing mechanisms may be overlooked in other species and that variable pollinator availability may play a significant role in the maintenance of mixed mating in species with delayed selfing, such as C. verna.

A life-history based study of population genetic structure: seed bank to adults in Plantago lanceolata

We explored the extent to which the soil seed bank differed genetically and spatially in comparison to two actively growing stages in a natural population of Plantago lanceolata. All seed‐bank seeds, seedlings, and adults of P. lanceolata within eight subunits in a larger population were mapped, subjected to starch gel electrophoresis, and allozyme analysis in 1988. Gel electrophoresis was also used to estimate the mating system in two years, 1986 and 1988. The spatial distributions of seeds, seedlings, and adults were highly coincident. Allele frequencies of the dormant seeds differed significantly from those of the adults for four of the five polymorphic loci. In addition, a comparison of the genotype frequencies of the three life‐history stages indicated that the seed bank had an excess of homozygotes. Homozygosity, relative to Hardy‐Weinberg expectations, decreased during the life cycle (for seed bank, seedlings, and adults respectively: Fit = 0.19, 0.09, 0.01; Fis = 0.14, 0.04, ‐0.12). Spatial genetic differentiation increased sixfold during the life cycle: (for seed bank, seedling and adults: Fs1∗∗∗ = 0.02, 0.05, 0.12). The apparent selfing rate was 0.01 in 1986 and 0.09 in 1988. These selfing rates are not large enough to account for the elevated homozygosity of the seed bank. Inbreeding depression, overdominance for fitness, and a “temporal Wahlunds effect” are discussed as possible mechanisms that could generate high homozygosity in the seed bank, relative to later life‐history stages. In Plantago lanceolata, the influence of the mating system and the “genetic memory” of the seed bank are obscured by the time plants reach the reproductive stage.