2005 Sewall Wright Award. Robert E. Ricklefs.
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Awards and Prizes↗
Biomedical subjects
Michael Turelli
Publications and source records attributed to Michael Turelli.
The geography of mammalian speciation: mixed signals from phylogenies and range maps.
The importance of geographic isolation in speciation has been debated since the 19th century. Since the beginning of the 20th century, the consensus has been that most speciation involves divergence in allopatry. This consensus was based largely on decades of observations by naturalists and verbal arguments against speciation without isolation. Recent attempts to quantify the importance of allopatric versus sympatric speciation using comparative methods called "age-range correlation" (ARC) suggest that allopatric speciation is more common than sympatric speciation. However, very few taxa have been studied and there are concerns about the adequacy of the methods. We propose methodological improvements including changes in the way overlap between clades is quantified and Monte Carlo methods to test the null hypothesis of no relationship between phylogenetic relatedness and geographic range overlap. We analyze 14 clades of mammals, chosen because of the availability of data and the consensus among mammalogists that speciation is routinely allopatric. Although data from a few clades clearly indicate allopatric speciation, divergence with gene flow is plausible in others and many results are inconclusive. The relative rarity of significant correlations between phylogenetic distance and range overlap may have three distinct causes: (1) post-speciation range changes, (2) relative rarity of range overlap, and (3) a mixture of geographic modes of speciation. Our results support skepticism about ARC's power for inferring the biogeography of speciation. Yet, even if few clades provide clear signals, meta-analytic approaches such as ARC may set bounds on the prevalence of alternative modes of speciation.
Animals↗
Will population bottlenecks and multilocus epistasis increase additive genetic variance?
We apply new analytical methods to understand the consequences of population bottlenecks for expected additive genetic variance. We analyze essentially all models for multilocus epistasis that have been numerically simulated to demonstrate increased additive variance. We conclude that for biologically plausible models, large increases in expected additive variance--attributable to epistasis rather than dominance--are unlikely. Naciri-Graven and Goudet (2003) found that as the number of epistatically interacting loci increases, additive variance tends to be inflated more after a bottleneck. We argue that this result reflects biologically unrealistic aspects of their models. Specifically, as the number of loci increases, higher-order epistatic interactions become increasingly important in these models, with an increasing fraction of the genetic variance becoming nonadditive, contrary to empirical observations. As shown by Barton and Turelli (2004), without dominance, conversion of nonadditive to additive variance depends only on the variance components and not on the number of loci per se. Numerical results indicating that more inbreeding is needed to produce maximal release of additive variance with more loci follow directly from our analytical results, which show that high levels of inbreeding (F > 0.5) are needed for significant conversion of higher-order components. We discuss alternative approaches to modeling multilocus epistasis and understanding its consequences.
Biological Evolution↗
Prediction of effects of genetic drift on variance components under a general model of epistasis.
For a model of diallelic loci with arbitrary epistasis, Barton and Turelli [2004. Effects of genetic drift on variance components under a general model of epistasis. Evolution 58, 2111-2132] gave results for variances among and within replicate lines obtained by inbreeding without selection. Here, we discuss the relation between their population genetic methods and classical quantitative genetic arguments. In particular, we consider the case of no dominance using classical identity by descent arguments, which generalizes their results from two alleles to multiple alleles. To clarify the connections between the alternative methods, we obtain the same results using an intermediate method, which explicitly identifies the statistical effects of sets of loci. We also discuss the effects of population bottlenecks on covariances among relatives.
Epistasis, Genetic↗
Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G x E interactions.
We investigate three alternative selection-based scenarios proposed to maintain polygenic variation: pleiotropic balancing selection, G x E interactions (with spatial or temporal variation in allelic effects), and sex-dependent allelic effects. Each analysis assumes an additive polygenic trait with n diallelic loci under stabilizing selection. We allow loci to have different effects and consider equilibria at which the population mean departs from the stabilizing-selection optimum. Under weak selection, each model produces essentially identical, approximate allele-frequency dynamics. Variation is maintained under pleiotropic balancing selection only at loci for which the strength of balancing selection exceeds the effective strength of stabilizing selection. In addition, for all models, polymorphism requires that the population mean be close enough to the optimum that directional selection does not overwhelm balancing selection. This balance allows many simultaneously stable equilibria, and we explore their properties numerically. Both spatial and temporal G x E can maintain variation at loci for which the coefficient of variation (across environments) of the effect of a substitution exceeds a critical value greater than one. The critical value depends on the correlation between substitution effects at different loci. For large positive correlations (e.g., rho(ij)2>3/4), even extreme fluctuations in allelic effects cannot maintain variation. Surprisingly, this constraint on correlations implies that sex-dependent allelic effects cannot maintain polygenic variation. We present numerical results that support our analytical approximations and discuss our results in connection to relevant data and alternative variance-maintaining mechanisms.
Data Interpretation, Statistical↗
Effects of genetic drift on variance components under a general model of epistasis.
We analyze the changes in the mean and variance components of a quantitative trait caused by changes in allele frequencies, concentrating on the effects of genetic drift. We use a general representation of epistasis and dominance that allows an arbitrary relation between genotype and phenotype for any number of diallelic loci. We assume initial and final Hardy-Weinberg and linkage equilibrium in our analyses of drift-induced changes. Random drift generates transient linkage disequilibria that cause correlations between allele frequency fluctuations at different loci. However, we show that these have negligible effects, at least for interactions among small numbers of loci. Our analyses are based on diffusion approximations that summarize the effects of drift in terms of F, the inbreeding coefficient, interpreted as the expected proportional decrease in heterozygosity at each locus. For haploids, the variance of the trait mean after a population bottleneck is var(delta(z)) = sigma(n)k=1 FkV(A(k)), where n is the number of loci contributing to the trait variance, V(A(1)) = V(A) is the additive genetic variance, and V(A(k)) is the kth-order additive epistatic variance. The expected additive genetic variance after the bottleneck, denoted (V*(A)), is closely related to var(delta(z)); (V*(A)) = (1 - F) sigma(n)k=1 kFk-1V(A(k)). Thus, epistasis inflates the expected additive variance above V(A)(1 - F), the expectation under additivity. For haploids (and diploids without dominance), the expected value of every variance component is inflated by the existence of higher order interactions (e.g., third-order epistasis inflates (V*(AA. This is not true in general with diploidy, because dominance alone can reduce (V*(A)) below V(A)(1 - F) (e.g., when dominant alleles are rare). Without dominance, diploidy produces simple expressions: var(delta(z)) = sigma(n)k=1 (2F)kV(A(k)) and (V(A)) = (1 - F) sigma(n)k=1 k(2F)k-1V(A(k)). With dominance (and even without epistasis), var(delta(z)) and (V*(A)) no longer depend solely on the variance components in the base population. For small F, the expected additive variance simplifies to (V*(A)) approximately equal to (1 - F)V(A) + 4FV(AA) + 2FV(D) + 2FC(AD), where C(AD) is a sum of two terms describing covariances between additive effects and dominance and additive X dominance interactions. Whether population bottlenecks lead to expected increases in additive variance depends primarily on the ratio of nonadditive to additive genetic variance in the base population, but dominance precludes simple predictions based solely on variance components. We illustrate these results using a model in which genotypic values are drawn at random, allowing extreme and erratic epistatic interactions. Although our analyses clarify the conditions under which drift is expected to increase V(A), we question the evolutionary importance of such increases.
Analysis of Variance↗
Stochasticity overrules the "three-times rule": genetic drift, genetic draft, and coalescence times for nuclear loci versus mitochondrial DNA.
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.
Cell Nucleus↗