Matings Systems and the Evolution of Niche Breadth.

OF THE DISSERTATION In order to predict how species will respond to global climate change, scientists must understand the relationships between traits, fitness, environments and distributions. Niche theory provides a useful framework. Niche breadth describes the range of environmental conditions necessary for population growth. Among these conditions, climate is especially important. Climate niche breadth in turn may reflect a confluence of different forces. This dissertation presents a series of projects that assess the relative roles of historical, geographic and population processes that contribute to climate niche breadth in temperate plants. The first project evaluates the predictive power of a classical hypothesis. If gene flow slows divergent adaptation, then range fragmentation should promote niche breadth. By quantifying the relationships between environmental difference, geographic distance and genetic isolation among European plants, I show that the effect of allopatry on niche breadth depends on the role of the geographic distance among populations. The remaining projects focus in increasingly finer detail on the evolution of niche breadth in a taxonomically complex group. Dodecatheon sect. Dodecatheon grow in diverse habitats across North America. They have confounded taxonomists with polyploidy, hybridization and convergent adaptation. Currently recognized species are either widespread or rare microclimate specialists. First, with multilocus phylogenetics, I show that the difference in niche breadth among rare and widespread species is not simply due to differences in environmental tolerance. In eastern North America, geographic heterogeneity and paleoclimate history strongly contribute to taxonomic rarity. The next project focuses on this group. Both rare eastern species are considered

Many of our theories for the generation and maintenance of diversity in nature depend on the existence of specialist biotic interactions which, in host–pathogen systems, also shape cross-species disease emergence. As such, niche breadth evolution, especially in host–parasite systems, remains a central focus in ecology and evolution. The predominant explanation for the existence of specialization in the literature is that niche breadth is constrained by trade-offs, such that a generalist is less fit on any particular environment than a given specialist. This trade-off theory has been used to predict niche breadth (co)evolution in both population genetics and eco-evolutionary models, with the different modelling methods providing separate, complementary insights. However, trade-offs may be far from universal, so population genetics theory has also proposed alternate mechanisms for costly generalism, including mutation accumulation. However, these mechanisms have yet to be integrated into eco-evolutionary models in order to understand how the mechanism of costly generalism alters the biological and ecological circumstances predicted to maintain specialism. In this review, we outline how population genetics and eco-evolutionary models based on trade-offs have provided insights for parasite niche breadth evolution and argue that the population genetics-derived mutation accumulation theory needs to be better integrated into eco-evolutionary theory.

Macroevolutionary and microevolutionary studies provide complementary explanations of the processes shaping the evolution of niche breadth. Macroevolutionary approaches scrutinize factors such as the temporal and spatial environmental heterogeneities that drive differentiation among species. Microevolutionary studies, in contrast, focus on the processes that affect intraspecific variability. We combine these perspectives by using macroevolutionary models in a comparative study of intraspecific variability. We address potential differences in rates of evolution of niche breadth and position in annual and perennial plants of the Eriogonoideae subfamily of the Polygonaceae. We anticipated higher rates of evolution in annuals than in perennials owing to differences in generation time that are paralleled by rates of molecular evolution. Instead, we found that perennial eriogonoid species present greater environmental tolerance (wider climate niche) than annual species. Niche breadth of perennial species has evolved two to four times faster than in annuals, while niche optimum has diversified more rapidly among annual species than among perennials. Niche breadth and average elevation of species are correlated. Moreover, niche breadth increases more rapidly with mean species elevation in perennials than in annuals. Our results suggest that both environmental gradients and life-history strategy influence rates and patterns of niche breadth evolution.

Bacteria exhibit varying niche breadths, with generalists thriving in diverse environments and specialists confined to specific habitats. Although genes for cooperative traits have been suggested to influence niche breadth evolution, their precise role remains unclear. We used a combination of phylogeny-based comparative methods to test causal hypotheses about the directionality of the relationship between genes for cooperation and bacterial niche breadth evolution across 25,785 species. Our results revealed 1) a positive correlation between the proportion of genes for cooperation and niche breadth; 2) genes for cooperation influenced niche breadth evolution, with a decreased proportion of such genes promoting niche contraction as the predominant evolutionary direction; and 3) genes for cooperation experience more frequent gain and loss within species rather than across species. These findings suggest a role of bacterial cooperation in influencing niche breadth evolution and maintaining the ecological versatility of bacteria. While our results are consistent with a simple relationship under the hypotheses tested, more complex causal scenarios are possible, including the role of factors that influence both cooperation and niche breadth.

Ecologists have long studied the evolution of niche breadth, including how variability in environments can drive the evolution of specialism and generalism. This concept is of particular interest in viruses, where niche breadth evolution may explain viral disease emergence, or underlie the potential for therapeutic measures like phage therapy. Despite the significance and potential applications of virus–host interactions, the genetic determinants of niche breadth evolution remain underexplored in many bacteriophages. In this study, we present the results of an evolution experiment with a model bacteriophage system, Escherichia virus T4, in several host environments: exposure to Escherichia coli C, exposure to E. coli K‐12, and exposure to both E. coli C and E. coli K‐12. This experimental framework allowed us to investigate the phenotypic and molecular manifestations of niche breadth evolution. First, we show that selection on different hosts led to measurable changes in phage productivity in all experimental populations. Second, whole—genome sequencing of experimental populations revealed signatures of selection. Finally, clear and consistent patterns emerged across the host environments, especially the presence of new mutations in phage structural genes—genes encoding proteins that provide morphological and biophysical integrity to a virus. A comparison of mutations found across functional gene categories revealed that structural genes acquired significantly more mutations than other categories. Our findings suggest that structural genes are central determinants in bacteriophage niche breadth.

Multi-model inference of non-random mating from an information theoretic approach

Sexual selection can be defined in terms of mating preferences which favour particular genotypes or phenotypes and which are expressed at the same level in all females without any degree of assortment in the matings. In this paper, population genetic models are analysed in which assortative mating is combined with sexual selection. If separate mating preferences for each of three genotypes at a locus give rise to sexual selection and if each genotype may also mate assortatively, then a wide range of conditions entails the establishment of a unique, globally stable equilibrium which coincides with the equilibrium for assortative mating alone. Under certain other conditions, however, one of two different stable equilibria will be established dependent on the parameters of both sexual selection and assortative mating. This multiplicity of equilibria cannot arise in models involving either sexual selection or assortative mating alone. If females prefer either dominant or recessive phenotypes, then the advent of sexual selection prohibits the fixation that would occur by assortative mating alone: the effect of sexual selection is to ensure that a globally stable equilibrium will be established. In the combined model, therefore, sexual selection for a dominant trait exerts a greater effect on the final outcome than assortative mating. However, in contradistinction to the model with dominance, assortative mating usually determines the outcome when genotypes are preferred and assort separately.

The MHC is one of the most polymorphic gene clusters in vertebrates and play an essential role in adaptive immunity. Apart from pathogen-mediated selection, sexual selection can also contribute to the maintenance of MHC diversity. MHC-dependent sexual selection could occur via several mechanisms but at present there is no consensus as to which of these mechanisms are involved and their importance. Previous studies have often suffered from limited genetic and behavioural data and small sample size, and were rarely able to examine all the mechanisms together, determine whether signatures of MHC-based non-random mating are independent of genomic effects or differentiate whether MHC-dependent sexual selection takes place at the pre- or post-copulatory stage. In this study, we use Monte Carlo simulation to investigate evidence for non-random MHC-dependent mating patterns by all three mechanisms in a free-living population of Soay sheep. Using 1710 sheep diplotyped at the MHC class IIa region and genome-wide SNPs, together with field observations of consorts, we found sexual selection against a particular haplotype in males at the pre-copulatory stage and sexual selection against female MHC heterozygosity during the rut. We also found MHC-dependent disassortative mating at the post-copulatory stage, along with strong evidence of inbreeding avoidance at both stages. However, results from generalized linear mixed models suggest that the pattern of MHC-dependent disassortative mating could be a by-product of inbreeding avoidance. Our results therefore suggest that while multiple apparent mechanisms of non-random mating with respect to the MHC may occur, some of them have alternative explanations.

Species distributions and their patterns in geographical space have been studied for several decades and explained by theories such as Janzen's, with respect to the nature of dispersal barriers in the Tropics, and Rapoport's, with respect to range size. However, the roles of specific environmental and geographical factors (e.g. ecological niche breadth, geographical barriers, etc.) in shaping species ranges and distributional patterns remain largely unexplored. The present study analyzed predictions from these two theories via analysis of virtual species with respect to biogeographical patterns: virtual species were created across South America, covering all major environments on the continent, and were used to compare effects of niche breadth, environmental availability, connectivity, seasonality, and the presence of known biogeographical barriers (rivers) in shaping species distributions and biodiversity patterns. Geographical ranges varied from narrow to broad, depending on the location of the seed point when comparing species produced with the same niche breadth. Analysis without consideration of seasonality and barriers produced species with broader distributions in the Tropics and narrower distributions in montane and temperate regions of the continent. When seasonality was included, however, broader ranges were concentrated in temperate regions, thus supporting Janzen's idea. Rapoport's rule of broader geographical ranges at higher latitudes was supported only when seasonality and physical barriers were included but not in species with very narrow or very broad niches, suggesting that this ‘rule’ results from interactions among niche breadth, dispersal capabilities, and dispersal barriers.

The evolution of female preferences for male display traits relies on females receiving indirect benefits from their mate. This requires substantial genetic variation in display traits or male quality. Nevertheless, sexual selection through mate choice has been assumed to deplete this genetic variation, ultimately diminishing preferences. However, sexual traits often have higher genetic variation than nonsexual traits. This contradiction, and, relatedly, how costly preferences and display traits are maintained, is called the "lek paradox." Using infinitesimal models and individual-based simulations, we show that variation in male traits and female preferences often mutually exaggerate each other under sexual selection, in a process analogous to runaway sexual selection but in terms of genetic variation. Therefore, contrary to prior suppositions, sexual selection may increase equilibrium genetic variance in display traits and preferences over that under random mating, provided that preference variance is not too small relative to trait variance. Increases in trait variance are more likely under directional than stabilizing preferences, but also occur under stabilizing preferences if preferences are not too weak. When mate choice does reduce trait variation, the effect is generally slight provided loci are highly polymorphic under random mating. However, when loci are already near fixation under random mating, increases or decreases in trait variance by mate choice become more pronounced due to changes in segregation variance. It is under situations such as lekking, where mate discrimination is effectively strong with weak fitness costs, that sexual selection may be most powerful in exaggerating male display variance.

Whether sexual selection impedes or aids adaptation has become an outstanding question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics. The net effect of sexual selection on population viability results from a balance between genetic benefits of “good‐genes” effects and costs of sexual conflict. Depending on how these facets of sexual selection are affected under environmental change, extinction of maladapted populations could be either avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes to disentangle the contributions of sexual selection, fecundity selection, and male–female coevolution to individual reproductive success and population fitness. We compared these contributions between the ancestral environment and two stressful environments (elevated temperature and a host plant shift). We found evidence that sexual selection on males had positive genetic effects on female fitness components across environments, supporting good‐genes sexual selection. Interestingly, however, when males evolved under sexual selection with fecundity selection removed, they became more robust to both temperature and host plant stress compared to their conspecific females and males from the other evolution regimes that applied fecundity selection. We quantified the population‐level consequences of this sex‐specific adaptation and found evidence that the cost of sociosexual interactions in terms of reduced offspring production was higher in the regime applying only sexual selection to males. Moreover, the cost tended to be more pronounced at the elevated temperature to which males from the regime were more robust compared to their conspecific females. These results illustrate the tension between individual‐level adaptation and population‐level viability in sexually reproducing species and suggest that the relative efficacies of sexual selection and fecundity selection can cause inherent sex differences in environmental robustness that may impact demography of maladapted populations.

Reproduction is costly and individual decisions about when and how much to invest in reproduction will relate to potential benefits in terms of offspring survivorship or mating success. For those organisms that can reproduce more than once, individuals should invest relatively more in reproduction when the potential benefits are high. If females gain directly or indirectly from choosing attractive, highly ornamented males, then it could be predicted that females mated to these males should invest more in reproduction. Here we report the first test of this prediction for a lekking species, peafowl (Pavo cristatus), in which males do not provide resources for offspring, and females prefer to mate with those males that possess the most elaborate trains. We find that peahens randomly mated to males that vary in the degree of ornament produce more eggs for those peacocks with more elaborate trains. We could find no evidence to support the possibility that this difference arises as a result of difference between males in their ability to fertilize eggs.

Comparisons of positive assortative mating and sexual selection models

The net effect of sexual selection on nonsexual fitness is controversial. On one side, elaborate display traits and preferences for them can be costly, reducing the nonsexual fitness of individuals possessing them, as well as their offspring. In contrast, sexual selection may reinforce nonsexual fitness if an individual's attractiveness and quality are genetically correlated. According to recent models, such good-genes mate choice should increase both the extent and rate of adaptation. We evolved 12 replicate populations of Drosophila serrata in a powerful two-way factorial experimental design to test the separate and combined contributions of natural and sexual selection to adaptation to a novel larval food resource. Populations evolving in the presence of natural selection had significantly higher mean nonsexual fitness when measured over three generations (13-15) during the course of experimental evolution (16-23% increase). The effect of natural selection was even more substantial when measured in a standardized, monogamous mating environment at the end of the experiment (generation 16; 52% increase). In contrast, and despite strong sexual selection on display traits, there was no evidence from any of the four replicate fitness measures that sexual selection promoted adaptation. In addition, a comparison of fitness measures conducted under different mating environments demonstrated a significant direct cost of sexual selection to females, likely arising from some form of male-induced harm. Indirect benefits of sexual selection in promoting adaptation to this novel resource environment therefore appear to be absent in this species, despite prior evidence suggesting the operation of good-genes mate choice in their ancestral environment. How novel environments affect the operation of good-genes mate choice is a fundamental question for future sexual selection research.

Insular species are predicted to broaden their niches, in response to having fewer competitors. They can thus exploit a greater proportion of the resource spectrum. In turn, broader niches are hypothesized to facilitate (or be a consequence of) increased population densities. We tested whether insular lizards have broader dietary niches than mainland species, how it relates to competitor and predator richness, and the nature of the relationship between population density and dietary niche breadth. We collected population density and dietary niche breadth data for 36 insular and 59 mainland lizard species, and estimated competitor and predator richness at the localities where diet data were collected. We estimated dietary niche shift by comparing island species to their mainland relatives. We controlled for phylogenetic relatedness, body mass and the size of the plots over which densities were estimated. We found that island and mainland species had similar niche breadths. Dietary niche breadth was unrelated to competitor and predator richness, on both islands and the mainland. Population density was unrelated to dietary niche breadth across island and mainland populations. Our results indicate that dietary generalism is not an effective way of increasing population density nor is it result of lower competitive pressure. A lower variety of resources on islands may prevent insular animals from increasing their niche breadths even in the face of few competitors.