Frequency-Dependent Selection Predicts Patterns of Radiations and Biodiversity

Negative frequency-dependent selection on polymorphic color morphs in adders

A well-documented pattern in the fossil record is a long-term decline in the origination rate of new taxa after diversity rebounds from a mass extinction. The mechanisms for this pattern remain elusive. In this article, we investigate the macroevolutionary predictions of an individual-based birth-death model (BDI model) where speciation and extinction rates emerge from population dynamics. We start with the simplest neutral model in which every individual has the same per capita rates of birth, death, and speciation. Although the prediction of the simplest neutral model agrees qualitatively with the fossil pattern, the predicted decline in per-species speciation rates is too fast to explain the long-term trend in fossil data. We thus consider models with variation among species in per capita rates of speciation and a suite of alternative assumptions about the heritability of speciation rate. The results show that interspecific variation in per capita speciation rate can induce differences among species in their ability to resist extinction because a low speciation rate confers a small but important demographic advantage. As a consequence, the model predicts an appropriately slow temporal decline in speciation rates, which provides a mechanistic explanation for the fossil pattern.

The topic of this thesis is the latitudinal diversity gradient: the general increase in numbers of species from high latitudes towards the equator. Although it is a well-documented and very general pattern, there is little consensus among biologists as to the causes of high tropical species richness. In Chapter 1 I give an overview of the latitudinal diversity gradient and hypotheses proposed to explain it, and outline a framework for developing and testing hypotheses. The emphasis in this thesis is on non-equilibrium hypotheses, and in particular on the idea that rates of species diversification are higher at low latitudes. In Chapter 2 I directly test the hypothesis that rates of species diversification increase towards the equator, using the phylogenetic method of sister-group comparisons. For birds and butterflies, 1 show that there does indeed appear to be an increase in rates of diversification towards lower latitudes. One possible explanation for this pattern links climatic conditions at low latitudes to faster speciation, via a causal chain which includes a higher rate of molecular evolution. In Chapter 3 I test the prediction that rates of molecular evolution are faster at low latitudes, using phylogenies reconstructed from DNA sequence data for birds. Although the results provide no evidence for a latitudinal effect on rates of cytb and ND2 evolution in birds, this chapter demonstrates a way in which further tests on a wider range of genes and taxa can be carried out as more sequence data becomes available. If rates of diversification are higher in the tropics, this may result from latitudinal gradients in life history traits which could influence rates of speciation or extinction. However, previous attempts to test for such patterns have rarely controlled for phylogenetic relationships among species, and have never controlled for geographic range overlap. In Chapter 4 I present a method for analyzing latitudinal variation in life history traits which takes both of these problems into account. For birds, this method indicates strong latitudinal variation in geographic range size and clutch size, less strong variation in body size and niche width, and no variation in the strength of sexual selection. While this does not prove that life history plays a part in generating the latitudinal diversity gradient, a robust demonstration of latitudinal variation in life history traits is an important prerequisite for any hypotheses which link life history with high tropical species richness. Speciation and extinction rates are believed to vary with species' life history and ecology. If speciation or extinction rates also vary with latitude, we should expect species with certain traits to show stronger latitudinal diversity gradients than others. We should also expect to see latitudinal variation in the macroecological structure of species assemblages. Chapters 5 and 6 confirm these expectations. In Chapter 5 I show that smaller-bodied bird species have steeper latitudinal diversity gradients than larger species. This is reflected in systematic latitudinal variation in the shape of body size frequency distributions, usually thought to be relatively consistent across regions. In Chapter 6 I show that body size - abundance relationships in the Australian marsupial fauna differ considerably between temperate and tropical subsets of the fauna. Whereas the temperate species display the typical negative relationship, the tropical species show no significant relationship. This pattern is consistent with the explanation that extinction rates vary with respect to body size, abundance and the latitude in which a species occurs. Together, the results of the analyses presented in this thesis provide evidence in favour of the non-equilibrium view that there are more species in the tropics because rates of species diversification are higher. It seems likely that this is due to latitudinal variation in environmental conditions, leading to latitudinal variation in species' life histories and the structure of species assemblages, and to latitudinal variation in rates of speciation or extinction. However, it is still difficult to judge whether it is variation in speciation rate (cradle model) or extinction rate (museum model) which is of primary importance, or if both are equally important. Further work on this question, applying the large-scale comparative methodology used here, will be necessary to progress towards a full understanding of the high species richness of the tropics.

Negative frequency-dependent selection among species is a key driver of community diversity in natural systems, but the degree to which negative frequency-dependent selection shapes patterns of survival and genetic diversity within species is poorly understood. In a 5-year field experiment, we show that seedlings of a tropical palm with rare genotypes had a pronounced survival advantage over seedlings with common genotypes, with effect sizes comparable to that of light availability. This 'rare genotype advantage' led to an increase in population-wide genetic diversity among seedlings compared to null expectations, as predicted by negative frequency-dependent selection, and increased reproductive success in adult trees with rare genotypes. These results suggest that within-species negative frequency-dependent selection of genotypes can shape genetic variation on ecologically relevant timescales in natural systems and may be a key, overlooked source of non-random mortality for tropical plants.

Large-scale patterns of species richness have been attributed to ecological limits, variation in diversification rates, and differences in evolutionary time, yet the relative importance of these drivers remains debated. Here, we present a unifying framework distinguishing four richness-generating scenarios, defined by contrasting roles of evolutionary time and speciation rates, which yields explicit and testable predictions for how evolutionary time, speciation, and environmental factors influence species richness. We applied this framework by analyzing 129 distinct, nonoverlapping clades spanning amphibians, reptiles, birds, and mammals. For each clade, we integrated historical biogeographic reconstructions, multiple estimates of speciation rates, and GIS-based environmental data. Using structural equation modeling, we quantified the direct and indirect effects of evolutionary time, speciation rates, and environmental conditions (productivity, temperature, and precipitation) on species richness. We further tested whether these effects varied systematically with clade-level traits, including age, physiology, diversity, and geographic extent. Productivity emerged as the dominant predictor of species richness, exerting strong and consistent direct effects that were largely invariant to clade traits. In contrast, speciation rates contributed little to species richness, while the influence of evolutionary time was highly context-dependent and most pronounced in younger clades. Temperature showed consistent direct effects not mediated by productivity, evolutionary time, or speciation rates, whereas precipitation influenced richness primarily via productivity. Together, our results support a productivity-driven equilibrium view of species richness, in which diversity reflects a balance between speciation and extinction regulated by energy availability. Deviations from equilibrium dynamics, particularly in younger clades, highlight the role of evolutionary history on biodiversity gradients.

Speciation can increase regional species richness, however, our knowledge of how and why speciation rates vary across space is still incomplete. Using comprehensive information on species distributions and their phylogenetic relationships, we describe the global spatial patterns of variation in amphibian speciation rates and explore their ecological determinants. We find that overall mean speciation rates in amphibians increase with latitude. This pattern is largely determined by anurans, the most diverse amphibian order. Salamanders, nevertheless, speciate faster in the tropics, whereas caecilians did not exhibit any relationship with latitude. Despite the overall inverse latitudinal trend in mean speciation rates of amphibians, tip-level maximum speciation rates are not necessarily restricted to higher latitudes and can be found in different regions across the globe. Among bioregions, higher mean speciation rates are associated with high past climatic velocity and topographic complexity, both factors potentially promoting isolation, an important primer for speciation. Our results suggest that the emerging inverse pattern of speciation rates in amphibians is likely driven by the combination of a few rapidly speciating clades distributed in higher latitudes and numerous clades in lower latitudes showing heterogeneous rates that, when averaged, pull down the estimations of mean speciation in the areas where they occur.

Rates of species formation vary widely across the tree of life and contribute to massive disparities in species richness among clades. This variation can emerge from differences in metapopulation-level processes that affect the rates at which lineages diverge, persist, and evolve reproductive barriers and ecological differentiation. For example, populations that evolve reproductive barriers quickly should form new species at faster rates than populations that acquire reproductive barriers more slowly. This expectation implicitly links microevolutionary processes (the evolution of populations) and macroevolutionary patterns (the profound disparity in speciation rate across taxa). Here, leveraging extensive field sampling from the Neotropical Cerrado biome in a biogeographically controlled natural experiment, we test the role of an important microevolutionary process-the propensity for population isolation-as a control on speciation rate in lizards and snakes. By quantifying population genomic structure across a set of codistributed taxa with extensive and phylogenetically independent variation in speciation rate, we show that broad-scale patterns of species formation are decoupled from demographic and genetic processes that promote the formation of population isolates. Population isolation is likely a critical stage of speciation for many taxa, but our results suggest that interspecific variability in the propensity for isolation has little influence on speciation rates. These results suggest that other stages of speciation-including the rate at which reproductive barriers evolve and the extent to which newly formed populations persist-are likely to play a larger role than population isolation in controlling speciation rate variation in squamates.

Sexual selection has been implicated as having a role in promoting speciation, as it should increase the rate of evolution of reproductive isolation, and there is some comparative evidence that sexual selection may be related to imbalances in clade size seen in resolved phylogenies. By employing a new comparative method we are able to investigate the role of sexual selection in explaining the patterns of species richness across birds. We used data for testes size as an index of post‐mating sexual selection, and sexual size dimorphism and sexual dichromatism as indices of pre‐mating sexual selection. These measures were obtained for 1031 species representing 467 genera. None of the variables investigated explained the patterns of species richness. As sexual selection may also increase extinction rates, the net effect on species richness in any given clade will depend on the balancing effects of sexual selection upon speciation and extinction rates. We suggest that variance across clades in this balance may have resulted in the lack of a relationship between species richness and sexual selection seen in birds.

Speciation Associated with Shifts in Migratory Behavior in an Avian Radiation.

Negative frequency-dependent selection (NFDS) is one of the most powerful selective forces maintaining genetic polymorphisms in nature. Recently many prospective cases of polymorphisms by NFDS have been reported. Some of them are very complicated, although strongly supportive of the NFDS. Here we investigate NFDS in wild populations of the dimorphic damselfly Ischnura senegalensis, in which females occur as andromorphs and gynomorphs. Specifically, we (1) test fitness responses to morph frequencies, (2) built a simple population genetic model, and (3) compare the observed and predicted morph-frequency dynamics. Fitnesses of the two morphs are an inverse function of its own frequency in a population, and are about equal when their frequencies are similar. Thus the conditions necessary for NFDS are satisfied. The long-term field surveys show that the morph frequencies oscillate with a period of two generations. Morph frequencies in a small population undergo large oscillations whereas those in a large population do small oscillations. The demographic properties of the observed dynamics agree well with those of our model. This example is one of the simplest confirmed cases of NFDS maintaining genetic polymorphisms in nature.

Positive selection on a new beneficial mutation generates a characteristic pattern of DNA sequence polymorphism when it reaches an intermediate allele frequency. On genome sequences of African Drosophila melanogaster, we detected such signatures of selection at 37 candidate loci and identified “sweeping haplotypes (SHs)” that are increasing or have increased rapidly in frequency due to hitchhiking. Based on geographic distribution of SH frequencies, we could infer whether selective sweeps occurred starting from de novo beneficial mutants under simple constant selective pressure. Single SHs were identified at more than half of loci. However, at many other loci, we observed multiple independent SHs, implying soft selective sweeps due to a high beneficial mutation rate or parallel evolution across space. Interestingly, SH frequencies were intermediate across multiple populations at about a quarter of the loci despite relatively low migration rates inferred between African populations. This invokes a certain form of frequency-dependent selection such as heterozygote advantage. At one locus, we observed a complex pattern of multiple independent that was compatible with recurrent frequency-dependent positive selection on new variants. In conclusion, genomic patterns of positive selection are very diverse, with equal contributions of hard and soft sweeps and a surprisingly large proportion of frequency-dependent selection in D. melanogaster populations.

Currently there is much interest in the potential for sexual selection or conflict to drive speciation. Theory proposes that speciation will be accelerated where sexual conflict is strong, particularly if females are ahead because mate choice will accentuate divergence by limiting gene flow. The Goodeinae are a monophyletic group of endemic Mexican fishes with an origin at least as old as the Miocene. Sexual selection is important in the Goodeinae and there is substantial interspecific variability in body morphology, which influences mate choice, allowing inference of the importance of female mate choice. We therefore used this group to test the relationship between sexual dimorphism and speciation rate. We quantified interspecific variation in sexual dimorphism amongst 25 species using a multivariate measure of total morphological differentiation between the sexes that accurately reflects sexual dimorphism driven by female mate choice and also used a mtDNA-based phylogeny to examine speciation rates. Comparative analyses failed to support a significant association between sexual dimorphism and speciation rate. In addition, variation in the time course of speciation throughout the whole clade was also examined using a similar tree containing 34 extant species. A constant rates model for the growth of this clade was rejected, but analyses instead indicated a decline in the rate of speciation over time. These results support the hypothesis of an early expansion of the group, perhaps due to an early radiation influenced by the key innovation of live bearing, or the prevalence of Miocene volcanism. In general, support for the role of sexual selection in generating patterns of speciation is proving equivocal and we argue that vicariance biogeography and adaptive radiations remain the most likely determinants of major patterns of diversification of continental organisms.

Accounting for the abundance of genetic variation in the face of natural selection remains a central problem of evolutionary biology. Genetic polymorphisms are constantly arising through mutation, and although most are promptly eliminated, polymorphisms in functionally important traits are common. One mechanism that can maintain polymorphisms is negative frequency-dependent selection on alternative alleles, whereby the fitness of each decreases as its frequency increases. Examples of frequency-dependent selection are rare, especially when attempting to describe the genetic basis of the phenotype under selection. Here we show frequency-dependent selection in a well-known natural genetic polymorphism affecting fruitfly foraging behaviour. When raised in low nutrient conditions, both of the naturally occurring alleles of the foraging gene (for(s) and for(R)) have their highest fitness when rare-the hallmark of negative frequency-dependent selection. This effect disappears at higher resources levels, demonstrating the role of larval competition. We are able to confirm the involvement of the foraging gene by showing that a sitter-like mutant allele on a rover background has similar frequency-dependent fitness as the natural sitter allele. Our study represents a clear demonstration of frequency-dependent selection, and we are able to attribute this effect to a single, naturally polymorphic gene known to affect behaviour.

Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates

Loci subject to negative frequency-dependent selection are expected to exhibit higher effective migration rates compared to reference loci. Although the number of gene copies transferred between populations by migration is the same for all genes, those subject to negative frequency-dependent selection are more likely to be retained in the immigrant population because rare alleles are selectively favored. So far, evidence for this prediction has been indirect, based on summary statistics rather than on migration rate estimates. Here, we introduce an approximate Bayesian procedure to jointly estimate migration rates at two predefined sets of loci between two populations. We applied the procedure to compare migration rate estimates at the self-incompatibility locus (S-locus) with that at 10 reference loci in two plant species, Leavenworthia alabamica and L. crassa (Brassicaceae). The maximum likelihood estimate for the proportion of migrants (m) was four times higher at the S-locus than at reference loci, but the difference was not statistically significant. Lack of significance might be due to insufficient data, but perhaps also to the recent divergence of the two species (311 ka), because we also show using simulations that the effective migration rate at the S-locus is expected to increase with increasing divergence time. These findings aid in understanding the evolutionary dynamics of negative frequency-dependent selection and they suggest that divergence time should be accounted for when employing migration rates to help detect negative frequency-dependent selection.