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ABSTRACT: Although coevolution is widely recognized as an important evolutionary process for pairs of reciprocally specialized species, its importance within species-rich communities of generalized species has been questioned. Here we develop and analyze mathematical models of mutualistic communities, such as those between plants and pollinators or plants and seed-dispersers to evaluate the importance of coevolutionary selection within complex communities. Our analyses reveal that coevolutionary selection can drive significant changes in trait distributions with important consequences for the network structure of mutualistic communities. One such consequence is greater connectance caused by an almost invariable increase in the rate of mutualistic interaction within the community. Another important consequence is altered patterns of nestedness. Specifically, interactions mediated by a mechanism of phenotype matching tend to be antinested when coevolutionary selection is weak and even more strongly antinested as increasing coevolutionary selection favors the emergence of reciprocal specialization. In contrast, interactions mediated by a mechanism of phenotype differences tend to be nested when coevolutionary selection is weak, but less nested as increasing coevolutionary selection favors greater levels of generalization in both plants and animals. Taken together, our results show that coevolutionary selection can be an important force within mutualistic communities, driving changes in trait distributions, interaction rates, and even network structure.
Evolution 02/2013; 67(2):338-54. · 5.15 Impact Factor
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ABSTRACT: The prevalence of polyploidy among flowering plants is surprising given the hurdles impeding the establishment and persistence of novel polyploid lineages. In the absence of strong assortative mating, reproductive assurance, or large intrinsic fitness advantages, new polyploid lineages face almost certain extinction through minority cytotype exclusion. Consequently, much work has focused on a search for adaptive advantages associated with polyploidy such as increased competitive ability, enhanced ecological tolerances, and increased resistance to pathogens. Yet, no consistent adaptive advantages of polyploidy have been identified. Here, to investigate the potential for autopolyploid establishment and persistence in the absence of any intrinsic fitness advantages, we develop a simulation model of a diploid population that sporadically gives rise to novel autopolyploids. The autopolyploids have only very small levels of initial assortative mating or niche differentiation, generated entirely by dosage effects of genome duplication, and they have realistic levels of reproductive assurance. Our results show that by allowing assortative mating and competitive interactions to evolve, establishment of novel autopolyploid lineages becomes common. Additional scenarios where adaptive optima change over time reveal that rapid environmental change promotes the replacement of diploid lineages by their autopolyploid descendants. These results help to explain recent empirical findings that suggest that many contemporary polyploid lineages arose during the Cretaceous-Tertiary extinction, without invoking adaptive advantages of polyploidy.
The American Naturalist 12/2011; 178(6):687-700. · 4.72 Impact Factor
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ABSTRACT: Newly formed polyploid lineages must contend with several obstacles to avoid extinction, including minority cytotype exclusion, competition, and inbreeding depression. If polyploidization results in immediate divergence of phenotypic characters these hurdles may be reduced and establishment made more likely. In addition, if polyploidization alters the phenotypic and genotypic associations between traits, that is, the P and G matrices, polyploids may be able to explore novel evolutionary paths, facilitating their divergence and successful establishment. Here, we report results from a study of the perennial plant Heuchera grossulariifolia in which the phenotypic divergence and changes in phenotypic and genotypic covariance matrices caused by neopolyploidization have been estimated. Our results reveal that polyploidization causes immediate divergence for traits relevant to establishment and results in significant changes in the structure of the phenotypic covariance matrix. In contrast, our results do not provide evidence that polyploidization results in immediate and substantial shifts in the genetic covariance matrix.
Evolution 12/2010; 65(6):1667-79. · 5.15 Impact Factor
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ABSTRACT: Coevolutionary interactions between species are thought to be an important cause of evolutionary diversification. Despite this general belief, little theoretical basis exists for distinguishing between the types of interactions that promote diversification and those types that have no effect or that even restrict it. Using analytical models and simulations of phenotypic evolution across a metapopulation, we show that coevolutionary interactions promote diversification when they impose a cost of phenotype matching, as is the case for competition or host-parasite antagonism. In contrast, classical coevolutionary arms races have no tendency to promote or inhibit diversification, and mutualistic interactions actually restrict diversification. Together with the results of recent phylogenetic and ecological studies, these results suggest that the causes of diversification in many coevolutionary systems may require reassessment.
The American Naturalist 10/2010; 176(6):802-17. · 4.72 Impact Factor
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ABSTRACT: Studying the correlation between traits of interacting species has long been a popular approach for identifying putative cases of coevolution. More recently, such approaches have been used as a means to evaluate support for the geographic mosaic theory of coevolution. Here we examine the utility of these approaches, using mathematical and computational models to predict the correlation that evolves between traits of interacting species for a broad range of interaction types. Our results reveal that coevolution is neither a necessary nor a sufficient condition for the evolution of spatially correlated traits between two species. Specifically, our results show that coevolutionary selection fails to consistently generate statistically significant correlations and, conversely, that non-coevolutionary processes can readily cause statistically significant correlations to evolve. In addition, our results demonstrate that studies of trait correlations per se cannot be used as evidence either for or against a geographic mosaic process. Taken together, our results suggest that understanding the coevolutionary process in natural populations will require detailed mechanistic studies conducted in multiple populations or the use of more sophisticated statistical approaches that better use information contained in existing data sets.
The American Naturalist 03/2010; 175(5):525-37. · 4.72 Impact Factor
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ABSTRACT: We analyze mathematical models to examine how the genetic basis of fitness affects the persistence of a population suddenly encountering a harsh environment where it would go extinct without evolution. The results are relevant for novel introductions and for an established population whose existence is threatened by a sudden change in the environment. The models span a range of genetic assumptions, including identical loci that contribute to absolute fitness, a two-locus quantitative genetic model with nonidentical loci, and a model with major and minor genes affecting a quantitative trait. We find as a general (though not universal) pattern that prospects for persistence narrow as more loci contribute to fitness, in effect because selection per locus is increasingly weakened with more loci, which can even overwhelm any initial enhancement of fitness that adding loci might provide. When loci contribute unequally to fitness, genes of small effect can significantly reduce extinction risk. Indeed, major and minor genes can interact synergistically to reduce the time needed to evolve growth. Such interactions can also increase vulnerability to extinction, depending not just on how genes interact but also on the initial genetic structure of the introduced, or newly invaded, population.
Evolutionary Applications 02/2010; 3(2):97 - 108. · 4.92 Impact Factor
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ABSTRACT: Interactions between gene flow, spatially variable selection, and genetic drift have long been a central focus of evolutionary research. In contrast, only recently has the potential importance of interactions between these factors for coevolutionary dynamics and the emergence of parasite local adaptation been realized. Here we study host-parasite coevolution in a metapopulation model when both the biotic and the abiotic components of the environment vary in space. We provide a general expression for parasite local adaptation that allows local adaptation to be partitioned into the contributions of spatial covariances between host and parasite genotype frequencies within and between habitats. This partitioning clarifies how relative rates of gene flow, spatially variable patterns of selection, and genetic drift interact to shape parasite local adaptation. Specifically, by using this expression in conjunction with coevolutionary models, we show that genetic drift can dramatically increase the level of parasite local adaptation under some models of specificity. We also show that the effect of migration on parasite local adaptation depends on the geographic mosaic of selection. We discuss how these predictions could be tested empirically or experimentally using microbial systems.
The American Naturalist 02/2009; 173(2):212-24. · 4.72 Impact Factor
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ABSTRACT: Interactions with parasites may promote the evolution of disassortative mating in host populations as a mechanism through which genetically diverse offspring can be produced. This possibility has been confirmed through simulation studies and suggested for some empirical systems in which disassortative mating by disease resistance genotype has been documented. The generality of this phenomenon is unclear, however, because existing theory has considered only a subset of possible genetic and mating scenarios. Here we present results from analytical models that consider a broader range of genetic and mating scenarios and allow the evolution of non-random mating in the parasite as well. Our results confirm results of previous simulation studies, demonstrating that coevolutionary interactions with parasites can indeed lead to the evolution of host disassortative mating. However, our results also show that the conditions under which this occurs are significantly more fickle than previously thought, requiring specific forms of infection genetics and modes of non-random mating that do not generate substantial sexual selection. In cases where such conditions are not met, hosts may evolve random or assortative mating. Our analyses also reveal that coevolutionary interactions with hosts cause the evolution of non-random mating in parasites as well. In some cases, particularly those where mating occurs within groups, we find that assortative mating evolves sufficiently to catalyze sympatric speciation in the interacting species.
Ecology Letters 09/2008; 11(9):937-46. · 17.56 Impact Factor
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ABSTRACT: A long-standing goal in evolutionary biology is to identify the conditions that promote the evolution of reproductive isolation and speciation. The factors promoting sympatric speciation have been of particular interest, both because it is notoriously difficult to prove empirically and because theoretical models have generated conflicting results, depending on the assumptions made. Here, we analyze the conditions under which selection favors the evolution of assortative mating, thereby reducing gene flow between sympatric groups, using a general model of selection, which allows fitness to be frequency dependent. Our analytical results are based on a two-locus diploid model, with one locus altering the trait under selection and the other locus controlling the strength of assortment (a "one-allele" model). Examining both equilibrium and nonequilibrium scenarios, we demonstrate that whenever heterozygotes are less fit, on average, than homozygotes at the trait locus, indirect selection for assortative mating is generated. While costs of assortative mating hinder the evolution of reproductive isolation, they do not prevent it unless they are sufficiently great. Assortative mating that arises because individuals mate within groups (formed in time or space) is most conducive to the evolution of complete assortative mating from random mating. Assortative mating based on female preferences is more restrictive, because the resulting sexual selection can lead to loss of the trait polymorphism and cause the relative fitness of heterozygotes to rise above homozygotes, eliminating the force favoring assortment. When assortative mating is already prevalent, however, sexual selection can itself cause low heterozygous fitness, promoting the evolution of complete reproductive isolation (akin to "reinforcement") regardless of the form of natural selection.
Genetics 08/2008; 179(4):2091-112. · 4.01 Impact Factor
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ABSTRACT: Theoretical and empirical studies of local adaptation in species interactions have increased greatly over the past decade, yielding new insights into the conditions that favor local adaptation or maladaptation. Generalizing the results of these studies is difficult, however, because of the different experimental designs that have been used to infer local adaptation. Particularly challenging is comparing results across empirical studies conducted in a common laboratory or garden environment with results of those conducted using transplants in natural environments. Here we develop simple and easily interpretable mathematical expressions for the quantities measured by these two different types of studies. Our results reveal that common-garden designs measure only a single component of local adaptation-the spatial covariance between the genotype frequencies of the interacting species-and thus provide only a partial description of local adaptation. In contrast, reciprocal-transplant designs incorporate additional terms that measure the contribution of spatial variability in the ecological environment. Consequently, the two types of studies should yield identical results only when local adaptation is caused by spatial variability in the genotype frequencies of the interacting species alone. In order to unify these disparate approaches, we develop a new methodology that can be used to estimate the individual components of local adaptation. When implemented in an appropriate experimental system, this partitioning allows the examination of fundamental questions such as the relative proportion of local adaptation attributable to interactions between species or to the abiotic environment.
The American Naturalist 06/2008; 171(5):658-68. · 4.72 Impact Factor
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ABSTRACT: Despite the well-documented historical importance of polyploidy, the mechanisms responsible for the establishment and evolutionary success of novel polyploid lineages remain unresolved. One possibility, which has not been previously evaluated theoretically, is that novel polyploid lineages are initially more resistant to pathogens than the diploid progenitor species. Here, we explore this possibility by developing and analysing mathematical models of interactions between newly formed polyploid lineages and their pathogens. We find that for the genetic mechanisms of pathogen resistance with the best empirical support, newly formed polyploid populations of hosts are expected to be more resistant than their diploid progenitors. This effect can be quite strong and, in the case of perennial species with recurrent polyploid formation, may last indefinitely, potentially providing a general explanation for the successful establishment of novel polyploid lineages.
Proceedings of the Royal Society B: Biological Sciences 11/2007; 274(1624):2393-7. · 5.41 Impact Factor
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ABSTRACT: Many well-studied coevolutionary interactions between predators and prey or hosts and parasites are mediated by quantitative traits. In some interactions, such as those between cuckoos and their hosts, interactions are mediated by the degree of phenotype matching among species, and a significant body of theory has been developed to predict the coevolutionary dynamics and outcomes of such interactions. In a large number of other cases, however, interactions are mediated by the extent to which the phenotype of one species exceeds that of the other. For these cases-which are arguably more numerous-few theoretical predictions exist for coevolutionary dynamics and outcomes. Here we develop and analyze mathematical models of interspecific interactions mediated by the extent to which the quantitative trait of one species exceeds that of the other. Our results identify important differences from previously studied models based on trait matching. First, our results show that cyclical dynamics are possible only if the strength of coevolutionary selection exceeds a threshold and stabilizing selection acts on the interacting traits. Second, our results demonstrate that significant levels of genetic polymorphism can be maintained only when cyclical dynamics occur. This result leads to the unexpected prediction that maintenance of genetic polymorphism is enhanced by strong selection. Finally, our results demonstrate that there is no a priori reason to expect the traits of interacting species should match in any literal sense, even in the absence of gene flow among populations.
Evolution 09/2007; 61(8):1823-34. · 5.15 Impact Factor
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ABSTRACT: The extent to which parasites are locally adapted to their hosts has important implications for human health and agriculture. A recently developed conceptual framework--the geographic mosaic theory of coevolution--predicts that local maladaptation should be common and largely determined by the interplay between gene flow and spatially variable reciprocal selection. Previous investigation of this theory has predominately focused on genetic systems of infection and resistance characterized by few genes of major effect and particular forms of epistasis. Here we extend existing theory by analyzing mathematical models of host-parasite interactions in which host resistance to parasites is mediated by quantitative traits with an additive polygenic basis. In contrast to previous theoretical studies predicated upon major gene mechanisms, we find that parasite local maladaptation is quite uncommon and restricted to one specific functional form of host resistance. Furthermore, our results show that local maladaptation should be rare or absent in studies that measure local adaptation using reciprocal transplant designs conducted in natural environments. Our results thus narrow the scope over which the predictions of the geographic mosaic theory are likely to hold and provide novel and readily testable predictions about when and where local maladaptation is expected.
Evolution 03/2007; 61(2):368-76. · 5.15 Impact Factor
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ABSTRACT: Coevolution between parasites and hosts or predators and prey often involves multiple species with similar kinds of defenses and counter-defenses. Classic examples include the interactions between phytophagous insects and their host plants, thick-shelled invertebrates and their shell-crushing predators, and ungulates and their predators. There are three major hypotheses for the nonequilibrium coevolutionary dynamics of these multispecific trophic interactions: escalation in traits, cycles in traits leading to fluctuating polymorphisms, and coevolutionary alternation. The conditions under which cycles and escalation are likely to occur have been well developed theoretically. In contrast, the conditions favoring coevolutionary alternation-evolutionary fluctuations in predator or prey preference driven by evolutionary shifts in relative levels of prey defense and vice versa-have yet to be identified. Using a set of quantitative coevolutionary models, we demonstrate that coevolutionary alternation can occur across a wide range of biologically plausible conditions. The result is often repeated, and potentially rapid, evolutionary shifts in patterns of specialization within networks of interacting species.
Evolution 12/2006; 60(11):2207-17. · 5.15 Impact Factor
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Scott L Nuismer
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ABSTRACT: A central prediction of the geographic mosaic theory of coevolution is that coevolving interspecific interactions will show varying degrees of local maladaptation. According to the theory, much of this local maladaptation is driven by selection mosaics and spatially intermingled coevolutionary hot and cold spots, rather than a simple balance between gene flow and selection. Here I develop a genetic model of host-parasite coevolution that is sufficiently general to incorporate selection mosaics, coevolutionary hot and cold spots, and a diverse array of genetic systems of infection/resistance. Results from this model show that the selection mosaics experienced by the interacting species are an important determinant of the sign and magnitude of local maladaptation. In some cases, this effect may be stronger than a previously described effect of relative rates of parasite and host gene flow. These results provide the first theoretical evidence that selection mosaics and coevolutionary hot and cold spots per se determine the magnitude and sign of local maladaptation. At the same time, however, these results demonstrate that coevolution in a geographic mosaic can lead to virtually any pattern of local adaptation or local maladaptation. Consequently, empirical studies that describe only patterns of local adaptation or maladaptation do not provide evidence either for or against the theory.
Evolution 02/2006; 60(1):24-30. · 5.15 Impact Factor
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ABSTRACT: Quantitative traits frequently mediate coevolutionary interactions between predator and prey or parasite and host. Previous efforts to understand and predict the coevolutionary dynamics of these interactions have generally assumed that standing genetic variation is fixed or absent altogether. We develop a genetically explicit model of coevolution that bridges the gap between these approaches by allowing genetic variation itself to evolve. Analysis of this model shows that the evolution of genetic variance has important consequences for the dynamics and outcome of coevolution. Of particular importance is our demonstration that coevolutionary cycles can emerge in the absence of stabilizing selection, an outcome not possible in previous models of coevolution mediated by quantitative traits. Whether coevolutionary cycles evolve depends upon the strength of selection, the number of loci, and the rate of mutation in each of the interacting species. Our results also generate novel predictions for the expected sign and magnitude of linkage disequilibria in each species.
Evolution 11/2005; 59(10):2073-82. · 5.15 Impact Factor
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ABSTRACT: Much of the diversity of flowering plants is associated with genomic duplication through polyploidy. Little is known, however, about the evolutionary mechanisms responsible for the diversification of novel polyploid lineages. We evaluated the possibility that divergence is driven by natural selection by estimating the strength of phenotypic selection acting on three floral traits in sympatric populations of diploid and autotetraploid Heuchera grossulariifolia over three years. Our results demonstrate consistent directional selection for increasing scape length and floral display in both diploid and tetraploid populations. In contrast, selection acting on flowering phenology varied across year and ploidy. Specifically, selection was found to favor late-flowering diploids in 2001 and 2002 but early-flowering tetraploids in 2003. We investigated the mechanistic basis of divergent selection for flowering phenology in 2003 by estimating the relationship between plant flowering phenology and the probability of intercytotype pollinator movement. The results demonstrated that less divergent tetraploids were significantly more likely to experience intercytotype flights than were more divergent tetraploids. This result is consistent with the pattern of phenotypic selection observed. Taken together, our results suggest that divergence of polyploids and their diploid progenitors may be driven by a process analogous to reinforcement whereby selection favors phenotypes that reduce the probability of intercytotype matings with reduced fertility.
Evolution 10/2005; 59(9):1928-35. · 5.15 Impact Factor
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ABSTRACT: Abstract Quantitative traits frequently mediate coevolutionary interactions between predator and prey or parasite and host. Previous efforts to understand and predict the coevolutionary dynamics of these interactions have generally assumed that standing genetic variation is fixed or absent altogether. We develop a genetically explicit model of coevolution that bridges the gap between these approaches by allowing genetic variation itself to evolve. Analysis of this model shows that the evolution of genetic variance has improtant consequences for the dyanmics and outcome of coevolution. Of particular importance is our demonstration that coevolutionary cycles can emerge in the absence of stabilizing selection, and outcome not possible in previous models of coevolution mediated by quantitative traits. whether coevolutionary cycles evolve depends upon the strength of selection, the number of loci, and the rate of mutation in each of the interacting species. Our results also generate novel predictions for the expected sign and magnitude of linkage disequilibria in each species.
Evolution 09/2005; 59(10):2073 - 2082. · 5.15 Impact Factor
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ABSTRACT: Interactions between hosts and parasites provide an ongoing source of selection that promotes the evolution of a variety of features in the interacting species. Here, we use a genetically explicit mathematical model to explore how patterns of gene expression evolve at genetic loci responsible for host resistance and parasite infection. Our results reveal the striking yet intuitive conclusion that gene expression should evolve along very different trajectories in the two interacting species. Specifically, host resistance loci should frequently evolve to co-express alleles, whereas parasite infection loci should evolve to express only a single allele. This result arises because hosts that co-express resistance alleles are able to recognize and clear a greater diversity of parasite genotypes. By the same token, parasites that co-express antigen or elicitor alleles are more likely to be recognized and cleared by the host, and this favours the expression of only a single allele. Our model provides testable predictions that can help interpret accumulating data on expression levels for genes relevant to host-parasite interactions.
PLoS Biology 08/2005; 3(7):e203. · 11.45 Impact Factor
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ABSTRACT: Although the majority of animals and plants, including humans, are dominated by the diploid phase of their life cycle, extensive diversity in ploidy level exists among eukaryotes, with some groups being primarily haploid whereas others alternate between haploid and diploid phases. Previous theory has illuminated conditions that favor the evolution of increased or decreased ploidy but has shed little light on which species should be primarily haploid and which primarily diploid. Here, we report a discovery that emerged from host-parasite models in which ploidy levels were allowed to evolve: selection is more likely to favor diploidy in host species and haploidy in parasite species. Essentially, when parasites must evade a host's immune system or defense response, selection favors parasitic individuals that express a narrow array of antigens and elicitors, thus favoring haploid parasites over diploid parasites. Conversely, when hosts must recognize a parasite before mounting a defensive response, selection favors hosts with a broader arsenal of recognition molecules, thus favoring diploid hosts over haploid hosts. These results are consistent with the predominance of haploidy among parasitic protists.
Proceedings of the National Academy of Sciences 08/2004; 101(30):11036-9. · 9.68 Impact Factor
