Mark W. Blows

Species borders: ecological and evolutionary perspectives

Recent ecological studies on species borders have used a number of approaches to establish causation for specific environmental factors and to identify the traits involved. These include interspecific comparisons, detailed investigations of marginal populations, and experimental manipulation. Species borders continue to be largely ignored in evolutionary biology, although some work suggests that marginal populations may often be relatively better-adapted to unfavourable conditions but perform poorly under most other conditions.

A REASSESSMENT OF GENETIC LIMITS TO EVOLUTIONARY CHANGE

An absence of genetic variance in traits under selection is perhaps the oldest explanation for a limit to evolutionary change, but has also been the most easily dismissed. We review a range of theoretical and empirical results covering single traits to more complex multivariate systems, and show that an absence of genetic variance may be more common than is currently appreciated. From a single-trait perspective, we highlight that it is becoming clear that some trait types do not display significant levels of genetic variation, and we raise the possibility that species with restricted ranges may differ qualitatively from more widespread species in levels of genetic variance in ecologically important traits. A common misconception in many life-history studies is that a lack of genetic variance in single traits, and genetic constraints as a consequence of bivariate genetic correlations, are different causes of selection limits. We detail how interpretations of bivariate patterns are unlikely to demonstrate genetic limits to selection in many cases. We advocate a multivariate definition of genetic constraints that emphasizes the presence (or otherwise) of genetic variance in the multivariate direction of selection. For multitrait systems, recent results using longer term studies of organisms, in which more is understood concerning what traits may be under selection, have indicated that selection may exhaust genetic variance, resulting in a limit to the selection response.

ESTIMATING NONLINEAR SELECTION GRADIENTS USING QUADRATIC REGRESSION COEFFICIENTS: DOUBLE OR NOTHING?

Abstract The use of regression analysis has been instrumental in allowing evolutionary biologists to estimate the strength and mode of natural selection. Although directional and correlational selection gradients are equal to their corresponding regression coefficients, quadratic regression coefficients must be doubled to estimate stabilizing/disruptive selection gradients. Based on a sample of 33 papers published in Evolution between 2002 and 2007, at least 78% of papers have not doubled quadratic regression coefficients, leading to an appreciable underestimate of the strength of stabilizing and disruptive selection. Proper treatment of quadratic regression coefficients is necessary for estimation of fitness surfaces and contour plots, canonical analysis of the γ matrix, and modeling the evolution of populations on an adaptive landscape.

A tale of two matrices: multivariate approaches in evolutionary biology

Two symmetric matrices underlie our understanding of microevolutionary change. The first is the matrix of nonlinear selection gradients (γ) which describes the individual fitness surface. The second is the genetic variance–covariance matrix (G) that influences the multivariate response to selection. A common approach to the empirical analysis of these matrices is the element‐by‐element testing of significance, and subsequent biological interpretation of pattern based on these univariate and bivariate parameters. Here, I show why this approach is likely to misrepresent the genetic basis of quantitative traits, and the selection acting on them in many cases. Diagonalization of square matrices is a fundamental aspect of many of the multivariate statistical techniques used by biologists. Applying this, and other related approaches, to the analysis of the structure of γ and G matrices, gives greater insight into the form and strength of nonlinear selection, and the availability of genetic variance for multiple traits.

Measuring Nonlinear Selection

A recent comprehensive review of empirical studies that measured the strength of selection concluded that there was little evidence for strong nonlinear selection in natural populations (Kingsolver et al. 2001). The median quadratic selection gradient identified by Kingsolver et al. (2001) was only 0.1, and gradients consistent with stabilizing or disruptive selection were found at a similar frequency and to be of similar magnitude. Stabilizing selection in particular is an important premise in many areas of evolutionary biology (Travis 1989), so this finding challenges our current understanding of how selection may operate in the wild (Conner 2001; Kingsolver et al. 2001). There is already some evidence that the strength and frequency of nonlinear selection identified in the review of Kingsolver et al. (2001) has influenced how evolutionary biologists view the potential role of stabilizing selection (Barton and Keightley 2002; Zhang et al. 2002). Kingsolver et al. (2001) suggest a number of reasons why empirical studies may not find or may underestimate nonlinear selection, including an empirical bias toward selecting experimental systems that are likely to show directional selection. In addition, nonlinear selection gradients are often able to be estimated from data sets but are not published (Kingsolver et al. 2001), probably as a consequence of the paucity of significant individual gradients and the difficulty of interpreting the overall pattern of nonlinear selection from the large number of estimated gradients. Here, we demonstrate that the strength of non-

Orientation of the Genetic Variance‐Covariance Matrix and the Fitness Surface for Multiple Male Sexually Selected Traits

Stabilizing selection has been predicted to change genetic variances and covariances so that the orientation of the genetic variance‐covariance matrix (G) becomes aligned with the orientation of the fitness surface, but it is less clear how directional selection may change G. Here we develop statistical approaches to the comparison of G with vectors of linear and nonlinear selection. We apply these approaches to a set of male sexually selected cuticular hydrocarbons (CHCs) of Drosophila serrata. Even though male CHCs displayed substantial additive genetic variance, more than 99% of the genetic variance was orientated 74.9° away from the vector of linear sexual selection, suggesting that open‐ended female preferences may greatly reduce genetic variation in male display traits. Although the orientation of G and the fitness surface were found to differ significantly, the similarity present in eigenstructure was a consequence of traits under weak linear selection and strong nonlinear (convex) selection. Associating the eigenstructure of G with vectors of linear and nonlinear selection may provide a way of determining what long‐term changes in G may be generated by the processes of natural and sexual selection.

Contrasting Mutual Sexual Selection on Homologous Signal Traits in Drosophila serrata

The nature of male mating preferences, and how they differ from female mating preferences in species with conventional sex roles, has received little attention in sexual selection studies. We estimated the form and strength of sexual selection as a consequence of male and female mating preferences in a laboratory‐based population of Drosophila serrata. The differences between sexual selection on male and female signal traits (cuticular hydrocarbons [CHCs]) were evaluated within a formal framework of linear and nonlinear selection gradients. Females tended to exert linear sexual selection on male CHCs, whereas males preferred intermediate female CHC phenotypes leading to convex (stabilizing) selection gradients. Possible mechanisms determining the nonlinear nature of sexual selection on female CHCs are proposed.

EXPERIMENTAL EVIDENCE FOR MULTIVARIATE STABILIZING SEXUAL SELECTION

Abstract Stabilizing selection is a fundamental concept in evolutionary biology. In the presence of a single intermediate optimum phenotype (fitness peak) on the fitness surface, stabilizing selection should cause the population to evolve toward such a peak. This prediction has seldom been tested, particularly for suites of correlated traits. The lack of tests for an evolutionary match between population means and adaptive peaks may be due, at least in part, to problems associated with empirically detecting multivariate stabilizing selection and with testing whether population means are at the peak of multivariate fitness surfaces. Here we show how canonical analysis of the fitness surface, combined with the estimation of confidence regions for stationary points on quadratic response surfaces, may be used to define multivariate stabilizing selection on a suite of traits and to establish whether natural populations reside on the multivariate peak. We manufactured artificial advertisement calls of the male cricket Teleogryllus commodus and played them back to females in laboratory phonotaxis trials to estimate the linear and nonlinear sexual selection that female phonotactic choice imposes on male call structure. Significant nonlinear selection on the major axes of the fitness surface was convex in nature and displayed an intermediate optimum, indicating multivariate stabilizing selection. The mean phenotypes of four independent samples of males, from the same population as the females used in phonotaxis trials, were within the 95% confidence region for the fitness peak. These experiments indicate that stabilizing sexual selection may play an important role in the evolution of male call properties in natural populations of T. commodus.

Divergent Selection and the Evolution of Signal Traits and Mating Preferences

Mating preferences are common in natural populations, and their divergence among populations is considered an important source of reproductive isolation during speciation. Although mechanisms for the divergence of mating preferences have received substantial theoretical treatment, complementary experimental tests are lacking. We conducted a laboratory evolution experiment, using the fruit fly Drosophila serrata, to explore the role of divergent selection between environments in the evolution of female mating preferences. Replicate populations of D. serrata were derived from a common ancestor and propagated in one of three resource environments: two novel environments and the ancestral laboratory environment. Adaptation to both novel environments involved changes in cuticular hydrocarbons, traits that predict mating success in these populations. Furthermore, female mating preferences for these cuticular hydrocarbons also diverged among populations. A component of this divergence occurred among treatment environments, accounting for at least 17.4% of the among-population divergence in linear mating preferences and 17.2% of the among-population divergence in nonlinear mating preferences. The divergence of mating preferences in correlation with environment is consistent with the classic by-product model of speciation in which premating isolation evolves as a side effect of divergent selection adapting populations to their different environments.

Levels of Mate Recognition Within and Between Two Drosophila Species and Their Hybrids

If sexual selection is to result in speciation, traits involved in mate choice within species need to be capable of producing sexual isolation between species. We investigated the association between mate choice and sexual isolation using interspecific hybrids between two sibling species, Drosophila serrata and Drosophila birchii. A perfuming experiment demonstrated that olfaction was involved in the sexual isolation between the two species. A quantitative genetic analysis using 30 populations of hybrids between the two species indicated that mating success in hybrid individuals was predominately determined by cuticular hydrocarbons; the average genetic correlation between mating success and cuticular hydrocarbon profile was 0.84, and in some instances exceeded 0.95. Multivariate analysis of the cuticular hydrocarbons of the two species revealed that there were three independent blends of cuticular hydrocarbons that separated three levels of organization: species, sex, and sex within species. The hydrocarbons used by hybrids in mate choice included those that separated the two species, demonstrating that species‐specific characters may be used in mate choice within populations. The interspecific reciprocal cross had major effect on which cuticular hydrocarbons were associated with mating success, indicating that the expression of the cuticular hydrocarbons was strongly sex linked.