Michael Turelli

Environmental Niche Equivalency versus Conservatism: Quantitative Approaches to Niche Evolution

Abstract Environmental niche models, which are generated by combining species occurrence data with environmental GIS data layers, are increasingly used to answer fundamental questions about niche evolution, speciation, and the accumulation of ecological diversity within clades. The question of whether environmental niches are conserved over evolutionary time scales has attracted considerable attention, but often produced conflicting conclusions. This conflict, however, may result from differences in how niche similarity is measured and the specific null hypothesis being tested. We develop new methods for quantifying niche overlap that rely on a traditional ecological measure and a metric from mathematical statistics. We reexamine a classic study of niche conservatism between sister species in several groups of Mexican animals, and, for the first time, address alternative definitions of “niche conservatism” within a single framework using consistent methods. As expected, we find that environmental niches of sister species are more similar than expected under three distinct null hypotheses, but that they are rarely identical. We demonstrate how our measures can be used in phylogenetic comparative analyses by reexamining niche divergence in an adaptive radiation of Cuban anoles. Our results show that environmental niche overlap is closely tied to geographic overlap, but not to phylogenetic distances, suggesting that niche conservatism has not constrained local communities in this group to consist of closely related species. We suggest various randomization tests that may prove useful in other areas of ecology and evolutionary biology.

Theory and speciation

The study of speciation has become one of the most active areas of evolutionary biology, and substantial progress has been made in documenting and understanding phenomena ranging from sympatric speciation and reinforcement to the evolutionary genetics of postzygotic isolation. This progress has been driven largely by empirical results, and most useful theoretical work has concentrated on making sense of empirical patterns. Given the complexity of speciation, mathematical theory is subordinate to verbal theory and generalizations about data. Nevertheless, mathematical theory can provide a useful classification of verbal theories; can help determine the biological plausibility of verbal theories; can determine whether alternative mechanisms of speciation are consistent with empirical patterns; and can occasionally provide predictions that go beyond empirical generalizations. We discuss recent examples of progress in each of these areas.

Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission

Genetic manipulations of insect populations for pest control have been advocated for some time, but there are few cases where manipulated individuals have been released in the field and no cases where they have successfully invaded target populations. Population transformation using the intracellular bacterium Wolbachia is particularly attractive because this maternally-inherited agent provides a powerful mechanism to invade natural populations through cytoplasmic incompatibility. When Wolbachia are introduced into mosquitoes, they interfere with pathogen transmission and influence key life history traits such as lifespan. Here we describe how the wMel Wolbachia infection, introduced into the dengue vector Aedes aegypti from Drosophila melanogaster, successfully invaded two natural A. aegypti populations in Australia, reaching near-fixation in a few months following releases of wMel-infected A. aegypti adults. Models with plausible parameter values indicate that Wolbachia-infected mosquitoes suffered relatively small fitness costs, leading to an unstable equilibrium frequency <30% that must be exceeded for invasion. These findings demonstrate that Wolbachia-based strategies can be deployed as a practical approach to dengue suppression with potential for area-wide implementation.

Heritable genetic variation via mutation-selection balance: Lerch's zeta meets the abdominal bristle.

Most quantitative traits in most populations exhibit heritable genetic variation. Lande proposed that high levels of heritable variation may be maintained by mutation in the face of stabilizing selection. Several analyses have appeared of two distinct models with n additive polygenic loci subject to mutation and stabilizing selection. Each is reviewed and a new analysis and model are presented. Lande and Fleming analyzed extensions of a model originally treated by Kimura which assumes a continuum of possible allelic effects at each locus. Latter and Bulmer analyzed a model with diallelic loci. The published analyses of these models lead to qualitatively different predictions concerning the dependence of the equilibrium genetic variance on the underlying biological parameters. A new asymptotic analysis of the Kimura model shows that the different predictions are not consequences of the number of alleles assumed but rather are attributable to assumptions concerning the relative magnitudes of per locus mutation rates, the phenotypic effects of mutation, and the intensity of selection. This conclusion is reinforced by analysis of a model with triallelic loci. None of the approximate analyses presented are mathematically rigorous. To quantify their accuracy and display the domains of validity for alternative approximations, numerically determined equilibria are presented. In addition, empirical estimates of mutation rates and selection intensity are reviewed, revealing weaknesses in both the data and its connection to the models. Although the mathematical results and underlying biological requirements of my analyses are quite different from those of Lande , the results do not refute his hypothesis that considerable additive genetic variance may be maintained by mutation-selection balance. However, I argue that the validity of this hypothesis can only be determined with additional data and mathematics.

THE EVOLUTION OF POSTZYGOTIC ISOLATION: ACCUMULATING DOBZHANSKY-MULLER INCOMPATIBILITIES

Abstract.— Hybrid sterility and inviability often result from the accumulation of substitutions that, while functional on their normal genetic backgrounds, cause a loss of fitness when brought together in hybrids. Previous theory has shown that such Dobzhansky‐Muller incompatibilities should accumulate at least as fast as the square of the number of substitutions separating two species, the so‐called snowball effect. Here we explicitly describe the stochastic accumulation of these incompatibilities as a function of time. The accumulation of these incompatibilities involves three levels of stochasticity: (1) the number of substitutions separating two allopatric lineages at a given time; (2) the number of incompatibilities resulting from these substitutions; and (3) the fitness effects of individual incompatibilities. Previous analyses ignored the stochasticity of molecular evolution (level 1) as well as that due to the variable effects of incompatibilities (level 3). Here we approximate the full stochastic process characterizing the accumulation of hybrid incompatibilities between pairs of loci. We derive the distribution of the number of incompatibilities as a function of divergence time between allopatric taxa as well as the distribution of waiting times to speciation by postzygotic isolation. We provide simple approximations for the mean and variance of these waiting times. These results let us estimate, albeit crudely, the probability, p, that two diverged sites from different species will contribute to hybrid sterility or inviability. Our analyses of data from Drosophila and Bombina suggest that p is generally very small, on the order of 10−6 or less.

PERSPECTIVE : A CRITIQUE OF SEWALL WRIGHT'S SHIFTING BALANCE THEORY OF EVOLUTION

We evaluate Sewall Wrights three‐phase “shifting balance” theory of evolution, examining both the theoretical issues and the relevant data from nature and the laboratory. We conclude that while phases I and II of Wrights theory (the movement of populations from one “adaptive peak” to another via drift and selection) can occur under some conditions, genetic drift is often unnecessary for movement between peaks. Phase III of the shifting balance, in which adaptations spread from particular populations to the entire species, faces two major theoretical obstacles: (1) unlike adaptations favored by simple directional selection, adaptations whose fixation requires some genetic drift are often prevented from spreading by barriers to gene flow; and (2) it is difficult to assemble complex adaptations whose constituent parts arise via peak shifts in different demes. Our review of the data from nature shows that although there is some evidence for individual phases of the shifting balance process, there are few empirical observations explained better by Wrights three‐phase mechanism than by simple mass selection. Similarly, artificial selection experiments fail to show that selection in subdivided populations produces greater response than does mass selection in large populations. The complexity of the shifting balance process and the difficulty of establishing that adaptive valleys have been crossed by genetic drift make it impossible to test Wrights claim that adaptations commonly originate by this process. In view of these problems, it seems unreasonable to consider the shifting balance process as an important explanation for the evolution of adaptations.

Phenotypic evolution, constant covariances, and the maintenance of additive variance

Theoretical work in evolutionary quantitative genetics concentrates on two problems: phenotypic evolution (including speciation) and the maintenance of the heritable variation on which evolution depends. I will argue that these problems are decoupled in practice, because detailed genetic models do not make useful predictions concerning the dynamics of the critical variance and covariance parameters that enter the evolution equations for means

STOCHASTICITY OVERRULES THE “THREE-TIMES RULE”: GENETIC DRIFT, GENETIC DRAFT, AND COALESCENCE TIMES FOR NUCLEAR LOCI VERSUS MITOCHONDRIAL DNA

Abstract Palumbi et al. (2001) proposed a “three-times rule” that uses mitochondrial DNA (mtDNA) sequences to predict probabilities of monophyly for nuclear loci (i.e., whether the alleles within a taxon coalesce with one another before they coalesce with alleles from a sister taxon). They use neutral coalescent theory to infer these probabilities from the ratio of interspecific divergence to intraspecific variation of mtDNA. We show that the estimated probabilities have very wide confidence intervals because of the inherent stochasticity of the mtDNA coalescent process. Under neutrality, the true probability of monophyly can be much higher, or much lower, than predicted by the three-times rule. We also review recent empirical and theoretical studies that refute neutrality-based predictions concerning mtDNA variation and divergence. We conclude that the three-times rule is neither a useful test for neutral molecular evolution nor a reliable guide to genealogical species.

EVOLUTION OF INCOMPATIBILITY-INDUCING MICROBES AND THEIR HOSTS

In many insect species, males infected with microbes related to Wolbachia pipientis are “incompatible” with uninfected females. Crosses between infected males and uninfected females produce significantly fewer adult progeny than the other three possible crosses. The incompatibility‐inducing microbes are usually maternally transmitted. Thus, incompatibility tends to confer a reproductive advantage on infected females in polymorphic populations, allowing these infections to spread. This paper analyzes selection on parasite and host genes that affect such incompatibility systems. Selection among parasite variants does not act directly on the level of incompatibility with uninfected females. In fact, selection favors rare parasite variants that increase the production of infected progeny by infected mothers, even if these variants reduce incompatibility with uninfected females. However, productivity‐reducing parasites that cause partial incompatibility with hosts harboring alternative variants can be favored once they become sufficiently abundant locally. Thus, they may spread spatially by a process analogous to the spread of underdominant chromosome rearrangements. The dynamics of modifier alleles in the host are more difficult to predict, because such alleles will occur in both infected and uninfected individuals. Nevertheless, the relative fecundity of infected females compared to uninfected females, the efficiency of maternal transmission and the mutual compatibility of infected individuals all tend to increase under within‐population selection on both host and parasite genes. In addition, selection on host genes favors increased compatibility between infected males and uninfected females. Although vertical transmission tends to harmonize host and parasite evolution, competition among parasite variants will tend to maintain incompatibility.

From Parasite to Mutualist: Rapid Evolution of Wolbachia in Natural Populations of Drosophila

Wolbachia are maternally inherited bacteria that commonly spread through host populations by causing cytoplasmic incompatibility, often expressed as reduced egg hatch when uninfected females mate with infected males. Infected females are frequently less fecund as a consequence of Wolbachia infection. However, theory predicts that because of maternal transmission, these “parasites” will tend to evolve towards a more mutualistic association with their hosts. Drosophila simulans in California provided the classic case of a Wolbachia infection spreading in nature. Cytoplasmic incompatibility allowed the infection to spread through individual populations within a few years and from southern to northern California (more than 700 km) within a decade, despite reducing the fecundity of infected females by 15%–20% under laboratory conditions. Here we show that the Wolbachia in California D. simulans have changed over the last 20 y so that infected females now exhibit an average 10% fecundity advantage over uninfected females in the laboratory. Our data suggest smaller but qualitatively similar changes in relative fecundity in nature and demonstrate that fecundity-increasing Wolbachia variants are currently polymorphic in natural populations.