Evolution

Published by Wiley
Online ISSN: 1558-5646
Publications
Lack of correlated evolution of methoxylated aromatics (left side) and pollination of Araceae (right side) in the Scarabaeidae. The P value from 1000 simulations in Pagels’ test of correlated evolution is 0.757. Phylogeny based on 18s ribosomal RNA (see section Methods for details). Note that only scarab genera with VOC data available are included in this analysis.
Araceae genera with data on floral VOC chemistry pollinated by scarab beetles.
Comparison of dated phylogenies of Scarabaeidae and Araceae (after Krell 2006) (scarabs), Nauheimer, Metzler, and Renner unpubl. ms. (aroids), with the reconstructed evolution of methoxylated aromatics indicated in red. In the aroids, the 95% highest posterior density interval of age estimation is given for the oldest split. The predicted oldest appearances of the other VOCs (classes) are indicated with names or abbreviations in the chronograms (MA = methoxylated aromatics; AA = aliphatic acyloins; FAE = fatty acid esters). Interactions through pollination are indicated with arrows. In the scarabs, bold lines begin with the oldest fossil record of the clade. Note that Anthurium and Spatiphyllum are partly pollinated by euglossine bees that also show preferences for some of the here analyzed VOCs such as MA.
Article
Coevolution is thought to be a major factor in shaping plant-pollinator interactions. Alternatively, plants may have evolved traits that fitted pre-existing preferences or morphologies in the pollinators. Here, we test these two scenarios in the plant family of Araceae and scarab beetles (Coleoptera, Scarabaeidae) as pollinators. We focused on floral volatile organic compounds (VOCs) and production/detection of VOCs by scarab beetles. We found phylogenetic structure in the production/detection of methoxylated aromatics in scarabs, but not plants. Within the plants, most of the compounds showed a well-supported pattern of correlated evolution with scarab-beetle pollination. In contrast, the scarabs showed no correlation between VOC production/detection and visitation to Araceae flowers, with the exception of the VOC skatole. Moreover, many VOCs were found in nonpollinating beetle groups (e.g., Melolonthinae) that are ancestors of pollinating scarabs. Importantly, none of the tested VOCs were found to have originated in pollinating taxa. Our analysis indicates a Jurassic origin of VOC production/detection in scarabs, but a Cretaceous/Paleocene origin of floral VOCs in plants. Therefore, we argue against coevolution, instead supporting the scenario of sequential evolution of floral VOCs in Araceae driven by pre-existing bias of pollinators.
 
Article
Genetic diversity at the S-locus controlling self-incompatibility (SI) is often high because of negative frequency-dependent selection. In species with highly patchy spatial distributions, genetic drift can overwhelm balancing selection and cause stochastic loss of S-alleles. Natural selection may favor the breakdown of SI in populations with few S-alleles because low S-allele diversity constrains the seed production of self-incompatible plants. We estimated S-allele diversity, effective population sizes, and migration rates in Leavenworthia alabamica, a self-incompatible mustard species restricted to discrete habitat patches in rocky glades. Patterns of polymorphism were investigated at the S-locus and 15 neutral microsatellites in three large and three small populations with 100-fold variation in glade size. Populations on larger glades maintained more S-alleles, but all populations were estimated to harbor at least 20 S-alleles, and mate availabilities typically exceeded 0.80, which is consistent with little mate limitation in nature. Estimates of the effective size (N(e)) in each population ranged from 600 to 1600, and estimated rates of migration (m) ranged from 3 x 10(-4) to nearly 1 x 10(-3). According to theoretical models, there is limited opportunity for genetic drift to reduce S-allele diversity in populations with these attributes. Although pollinators or resources limit seed production in small glades, limited S-allele diversity does not appear to be a factor promoting the incipient breakdown of SI in populations of this species that were studied.
 
Article
The evolutionary analysis of community organization is considered a major frontier in biology. Nevertheless, current explanations for community structure exclude the effects of genes and selection at levels above the individual. Here, we demonstrate a genetic basis for community structure, arising from the fitness consequences of genetic interactions among species (i.e., interspecific indirect genetic effects or IIGEs). Using simulated and natural communities of arthropods inhabiting North American cottonwoods (Populus), we show that when species comprising ecological communities are summarized using a multivariate statistical method, nonmetric multidimensional scaling (NMDS), the resulting univariate scores can be analyzed using standard techniques for estimating the heritability of quantitative traits. Our estimates of the broad-sense heritability of arthropod communities on known genotypes of cottonwood trees in common gardens explained 56-63% of the total variation in community phenotype. To justify and help interpret our empirical approach, we modeled synthetic communities in which the number, intensity, and fitness consequences of the genetic interactions among species comprising the community were explicitly known. Results from the model suggest that our empirical estimates of broad-sense community heritability arise from heritable variation in a host tree trait and the fitness consequences of IGEs that extend from tree trait to arthropods. When arthropod traits are heritable, interspecific IGEs cause species interactions to change, and community evolution occurs. Our results have implications for establishing the genetic foundations of communities and ecosystems.
 
Similarity in preferences between pairs of genetic sisters and pairs of foster sisters. The preferences were measured as the proportion of time spent with the focal male in a two-way choice chamber. They were normalized by angular transformation (y’= arcsine(√y)) for display and analysis, but percentage-scale labels are shown in the plots. Forty-four pairs of genetic sisters and 44 pairs of foster sisters were tested with eight sets of two males each. Regression lines are shown for each pair of sisters. The black data points and the solid black regression line highlight a typical example (one close to the population mean) for the eight pairs of trials of one pair of sisters.
Between-female agreement in mate choices in a two-way choice chamber. Each female had eight trials and proportion of agreements in dichotomized preferences (identity of the male that a female spent the larger fraction of time with) was calculated between pairs of genetic sisters, pairs of foster sisters and pairs of unrelated females. The three plots show all trials (A), only trials with time allocation to the preferred male of >70% (B), and only trials with time allocation to the preferred male of >85% (C). Because limiting the comparisons to only clear choices means excluding trials with less clear choices, sample sizes vary among plots. Differences between the agreement among genetic sisters and the agreement among foster sisters relative to the agreement among unrelated females were tested in a generalized linear model (GLM) with binomial error structure and logit link and a single categorical predictor (type of female pair) with three levels. P-values refer to the contrasts between the two types of females and the reference category (unrelated females).
Article
Many species show substantial between-individual variation in mating preferences, but studying the causes of such variation remains a challenge. For example, the relative importance of heritable variation versus shared early environment effects (like sexual imprinting) on mating preferences has never been quantified in a population of animals. Here, we estimate the heritability of and early rearing effects on mate choice decisions in zebra finches based on the similarity of choices between pairs of genetic sisters raised apart and pairs of unrelated foster sisters. We found a low and nonsignificant heritability of preferences and no significant shared early rearing effects. A literature review shows that a low heritability of preferences is rather typical, whereas empirical tests for the relevance of sexual imprinting within populations are currently limited to very few studies. Although effects on preference functions (i.e., which male to prefer) were weak, we found strong individual consistency in choice behavior and part of this variation was heritable. It seems likely that variation in choice behavior (choosiness, responsiveness, sampling behavior) would produce patterns of nonrandom mating and this might be the more important source of between-individual differences in mating patterns.
 
Article
Understanding how genetic variation shapes species' distributions involves examining how variation is distributed across a species' range as well as how it responds to underlying environmental heterogeneity. We examined patterns of fitness variation across the local distribution of an annual composite (Lasthenia fremontii) spanning a small-scale inundation gradient in a California vernal pool wetland. Using seeds collected from the center and edge of a population, paternal half-sib families were generated and transplanted back to the center and edge of the original population. All transplants were adapted to the conditions at the center of the population. The effect of the environment on the opportunity for selection depended on the model of selection assumed. Under a model of hard selection, variance in absolute fitness was lower among transplants at the edge of the population than at the center. Under a model of soft selection, the variance in relative fitness was similar between center and edge microhabitats. Given that this population is likely well-mixed, differences in habitat quality between center and edge microhabitats will likely cause selection at the center of the population to dominate the evolutionary trajectory of this population.
 
Examples of the diversity of insect–microbe mutualistic interactions. (A) A female Acyrthosiphon pisum (Hemiptera: Aphididae) and her offspring. (N. Moran, University of Arizona) (B) Cells of Buchnera aphidicola from A. pisum localized in a specialized cell known as a mycetocyte. (N. Moran, University of Arizona) (C) A female Megacopta punctatissima (Hemiptera: Plataspidae) depositing eggs and symbiont capsules in the field. (T. Hosokawa, National Institute of Advanced Industrial Science and Technology, Japan) (D) Candidtatus Ishikawaella capsulata cells in midgut of a female M. punctatissima. (T. Hosokawa, National Institute of Advanced Industrial Science and Technology, Japan) (E) Asteromyia carbonifera (Diptera: Cecidomyiidae) resting on a leaf of its host plant, Solidago sp. (J. Stireman, Wright State University) (F) Examples of A. carbonifera galls; gall structure can be partially attributed to the fungal symbiont Botryosphaeria sp. (P. Abbot, Vanderbilt University).
(A) The traditional model of an adaptive evolutionary 
A)Hatched box: radiations of phytophagous insects occur via shifts onto novel host plant species on which they are competitively and evolutionarily viable (ecological opportunity is present) and between which divergent selection occurs (selective trade-offs are present). (B) The ecological opportunity and selective trade-offs experienced by microbial symbionts must be taken into account when considering the adaptive radiations of insect–microbe mutualisms. Stippled box: Conditions favorable for the radiation of microbial partners can promote (✓) or hinder (X) the radiation of insect hosts otherwise possessing or lacking the appropriate ecological opportunities. Other configurations for the axes and/or new axes are easily imaginable (e.g., an axis for other trophic interactions, such as natural enemies, could be added).
Article
Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect-microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.
 
Article
Quantitative genetics is at or is fast approaching its centennial. In this perspective I consider five current issues pertinent to the application of quantitative genetics to evolutionary theory. First, I discuss the utility of a quantitative genetic perspective in describing genetic variation at two very different levels of resolution, (1) in natural, free-ranging populations and (2) to describe variation at the level of DNA transcription. Whereas quantitative genetics can serve as a very useful descriptor of genetic variation, its greater usefulness is in predicting evolutionary change, particularly when used in the first instance (wild populations). Second, I review the contributions of Quantitative trait loci (QLT) analysis in determining the number of loci and distribution of their genetic effects, the possible importance of identifying specific genes, and the ability of the multivariate breeder's equation to predict the results of bivariate selection experiments. QLT analyses appear to indicate that genetic effects are skewed, that at least 20 loci are generally involved, with an unknown number of alleles, and that a few loci have major effects. However, epistatic effects are common, which means that such loci might not have population-wide major effects: this question waits upon (QTL) analyses conducted on more than a few inbred lines. Third, I examine the importance of research into the action of specific genes on traits. Although great progress has been made in identifying specific genes contributing to trait variation, the high level of gene interactions underlying quantitative traits makes it unlikely that in the near future we will have mechanistic models for such traits, or that these would have greater predictive power than quantitative genetic models. In the fourth section I present evidence that the results of bivariate selection experiments when selection is antagonistic to the genetic covariance are frequently not well predicted by the multivariate breeder's equation. Bivariate experiments that combine both selection and functional analyses are urgently needed. Finally, I discuss the importance of gaining more insight, both theoretical and empirical, on the evolution of the G and P matrices.
 
Article
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.
 
Article
The most enigmatic sexual manipulation by Wolbachia endosymbionts is cytoplasmic incompatibility (CI): infected males are reproductively incompatible with uninfected females. In this paper, we extend the theory on population dynamics and evolution of CI, with emphasis on haplodiploid species. First, we focus on the problem of the threshold to invasion of the Wolbachia infection in a population. Simulations of the dynamics of infection in small populations show that it does not suffice to assume invasion by drift alone (or demographic "accident"). We propose several promising alternatives that may facilitate invasion of Wolbachia in uninfected populations: sex-ratio effects, meta population structure, and other fitness-compensating effects. Including sex-ratio effects of Wolbachia allows invasion whenever infected females produce more infected daughters than uninfected females produce uninfected daughters. Several studies on haplodiploid species suggest the presence of such sex-ratio effects. The simple metapopulation model we analyzed predicts that, given that infecteds are better "invaders," uninfecteds must be better "colonizers" to maintain coexistence of infected and uninfected patches. This condition seems more feasible for species that suffer local extinction due to predation (or parasitization) than for species that suffer local extinction due to overexploiting their resource(s). Finally, we analyze the evolution of CI in haplodiploids once a population has been infected. Evolution does not depend on the type of CI (female mortality or male production), but hinges solely on decreasing the fitness cost and/or increasing the transmission efficiency. Our models offer new perspectives for increasing our understanding of the population and evolutionary dynamics of CI.
 
Article
Few studies have examined genotype by environment (GxE) effects on premating reproductive isolation and associated behaviors, even though such effects may be common when speciation is driven by adaptation to different environments. In this study, mating success and courtship song differences among diverging populations of Drosophila mojavensis were investigated in a two-environment quantitative trait locus (QTL) analysis. Baja California and mainland Mexico populations of D. mojavensis feed and breed on different host cacti, so these host plants were used to culture F2 males to examine host-specific QTL effects and GxE interactions influencing mating success and courtship songs. Linear selection gradient analysis showed that mainland females mated with males that produced songs with significantly shorter L(long)-IPIs, burst durations, and interburst intervals. Twenty-one microsatellite loci distributed across all five major chromosomes were used to localize effects of mating success, time to copulation, and courtship song components. Male courtship success was influenced by a single detected QTL, the main effect of cactus, and four GxE interactions, whereas time to copulation was influenced by three different QTLs on the fourth chromosome. Multiple-locus restricted maximum likelihood (REML) analysis of courtship song revealed consistent effects linked with the same fourth chromosome markers that influenced time to copulation, a number of GxE interactions, and few possible cases of epistasis. GxE interactions for mate choice and song can maintain genetic variation in populations, but alter outcomes of sexual selection and isolation, so signal evolution and reproductive isolation may be slowed in diverging populations. Understanding the genetics of incipient speciation in D. mojavensis clearly depends on cactus-specific expression of traits associated with courtship behavior and sexual isolation.
 
Article
The evolution of antibiotic resistance provides a well-documented, rapid, and recent example of a selection driven process that has occurred in many bacterial species. An exhaustive collection of Moraxella catarrhalis that spans a transition to chromosomally encoded penicillin resistance was used to analyze genetic changes accompanying the transition. The population was characterized by high haplotypic diversity with 148 distinct haplotypes among 372 isolates tested at three genomic regions. The power of a temporally stratified sample from a single population was highlighted by the finding of high genetic diversity throughout the transition to resistance, population numbers that remained high over time, and no evidence of departures from neutrality in the allele frequency spectra throughout the transition. The direct temporal analysis documented the persistence, antibiotic status, and haplotypic identity of strains undergoing apparent clonal expansions. Several haplotypes that were beta-lactamase nonproducers in early samples converted to producers in later years. Maintenance of genetic diversity and haplotype conversions from sensitive to resistant supported the hypothesis that penicillin resistance determinants spread to a diverse array of strains via horizontal exchange. Genetic differentiation between sample years, estimated by F(ST), was increasing at a rate that could cause complete haplotype turnover in less than 150 years. Widespread linkage disequilibrium among sites within one locus (copB) suggested recent mutation followed by clonal expansion. Nonrandom associations between haplotypes and resistance phenotypes provided further evidence of clonal expansion for some haplotypes. Nevertheless, the population structure was far from clonal as evidenced by a relatively low frequency of disequilibria both within sites at a second locus (M46) as well as between loci. The haplotype-antibiotic resistance association that was accompanied by gradual haplotype turnover is consistent with a hypothesis of genetic drift at marker loci with directional selection at the resistance locus.
 
Article
The production of public goods by the contribution of individual volunteers is a social dilemma because an individual that does not volunteer can benefit from the public good produced by the contributions of others. Therefore it is generally believed that public goods can be produced only in the presence of repeated interactions (which allow reciprocation, reputation effects and punishment) or relatedness (kin selection). Cooperation, however, often occurs in the absence of iterations and relatedness. We show that when the production of a public good is a Volunteer's Dilemma, in which a fixed number of cooperators is necessary to produce the public good, cooperators and defectors persist in a mixed equilibrium, without iterations and without relatedness. This mixed equilibrium is absent in the N-person Prisoner's Dilemma, in which the public good is a linear function of the individual contributions. We also show that the Prisoner's Dilemma and the Volunteer's Dilemma are the two opposite extremes of a general public goods game, and that all intermediate cases can have a mixed equilibrium like the Volunteer's Dilemma. The coexistence of cooperators and defectors, therefore, is a typical outcome of most social dilemmas, which requires neither relatedness nor iterations.
 
Article
If two previously isolated taxa mutually assimilate through hybridization and subsequent biparental introgression, and if their introgressed descendants have the same or higher fitness than their parents, then gene flow should result in the local extinction of parental taxa via replacement by hybrid derivatives. These dramatic events may occur rapidly, even in a few generations. Given the speed at which such extinction by hybridization may occur, it may be difficult to identify that the process has occurred. Thus, documented instances of extinction by hybridization are rare, and especially so for cases in which both parents are replaced by the hybrid lineage. Here we report morphological and allozyme evidence for the local extinction of two Raphanus species in California via replacement by their hybrid-derived descendants. The results from a greenhouse experiment demonstrate that California wild radishes have a specific combination of traits from their progenitors, and comparison of our results to that of an earlier report indicate that pure parental types are no longer present in the wild. Our results also show the hybrid-derived lineage has transgressive fruit weight compared to its parents. Allozyme analysis demonstrates that California wild radishes are derived from hybridization between the putative parental species. However, that analysis also demonstrates that California wild radish has now become an evolutionary entity separate from both of its parents. We suggest that the aggressive colonizing behavior of the hybrid-derived lineage probably results from a novel combination of parental traits, rather than genetic variability of the population per se.
 
Article
Analyses among animal species have found that reproductive isolation increases monotonically with genetic distance, evolves more quickly for prezygotic than postzygotic traits, and is stronger among sympatric than allopatric species pairs. The latter pattern is consistent with expectations under the reinforcement hypothesis. To determine whether similar trends are found among plant species, patterns of reproductive isolation (postpollination prezygotic, postzygotic, and "total" isolation) in three plant genera (Glycine, Silene, Streptanthus) were examined using data from previously published artificial hybridization experiments. In Silene, all measures of reproductive isolation were positively correlated with genetic distance. In contrast, in Glycine and Streptanthus, correlations between reproductive isolation and genetic distance were weak or nonsignificant, possibly due to the influence of biologically unusual taxa, variable evolutionary forces acting in different lineages, or insufficient time to accumulate reproductive isolation. There was no evidence that postpollination prezygotic reproductive isolation evolved faster than postzygotic isolation in Glycine or Silene. We also detected no evidence for faster accumulation of postmating prezygotic isolation between sympatric than allopatric species pairs; thus we found no evidence for the operation of speciation via reinforcement. In Silene, which included six polyploid species, results suggest that changes in ploidy disrupt a simple monotonic relationship between isolation and genetic distance.
 
Article
Multiple mating by females (polyandry) remains hard to explain because, while it has substantial costs, clear benefits have remained elusive. The problem is acute in the social insects because polyandry is probably particularly costly for females and most material benefits of the behavior are unlikely to apply. It has been suggested that a fitness benefit may arise from the more genetically diverse worker force that a polyandrous queen will produce. One leading hypothesis is that the increased genetic diversity of workers will improve a colony's resistance to disease. We investigated this hypothesis using a polyandrous leaf-cutting ant and a virulent fungal parasite as our model system. At high doses of the parasite most patrilines within colonies were similarly susceptible, but a few showed greater resistance. At a low dose of the parasite there was more variation between patrilines in their resistance to the parasite. Such genetic variation is a key prerequisite for polyandry to result in increased disease resistance of colonies. The relatedness of two hosts did not appear to affect the transmission of the parasite between them, but this was most likely because the parasite tested was a virulent generalist that is adapted to transmit between distantly related hosts. The resistance to the parasite was compared between small groups of ants of either high or low genetic diversity. No difference was found at high doses of the parasite, but a significant improvement in resistance in high genetic diversity groups was found at a low dose of the parasite. That there is genetic variation for disease resistance means that there is the potential for polyandry to produce more disease-resistant colonies. That this genetic variation can improve the resistance of groups even under the limited conditions tested suggests that polyandry may indeed produce colonies with improved resistance to disease.
 
Article
Introgressive hybridization is an important evolutionary process and new analytical methods provide substantial power to detect and quantify it. In this study we use variation in the frequency of 657 AFLP fragments and DNA sequence variation from 15 genes to measure the extent of admixture and the direction of interspecific gene flow among three Heliconius butterfly species that diverged recently as a result of natural selection for Miillerian mimicry, and which continue to hybridize. Bayesian clustering based on AFLP genotypes correctly delineated the three species and identified four H. cydno, three H. pachinus, and three H. melpomene individuals that were of mixed ancestry. Gene genealogies revealed substantial shared DNA sequence variation among all three species and coalescent simulations based on the Isolation with Migration (IM) model pointed to interspecific gene flow as its cause. The IM simulations further indicated that interspecific gene flow was significantly asymmetrical, with greater gene flow from H. pachinus into H. cydno (2Nm = 4.326) than the reverse (2Nm = 0.502), and unidirectional gene flow from H. cydno and H. pachinus into H. melpomene (2Nm = 0.294 and 0.252, respectively). These asymmetries are in the directions expected based on the genetics of wing patterning and the probability that hybrids of various phenotypes will survive and reproduce in different mimetic environments. This empirical demonstration of extensive interspecific gene flow is in contrast to a previous study which found little evidence of gene flow between another pair of hybridizing Heliconius species, H. himera and H. erato, and it highlights the critical role of natural selection in maintaining species diversity. Furthermore, these results lend support to the hypotheses that phenotypic diversification in the genus Heliconius has been fueled by introgressive hybridization and that reinforcement has driven the evolution of assortative mate preferences.
 
Article
Discoveries of mutations conferring resistance to infectious diseases have led to increased interest in the evolutionary dynamics of disease resistance. Several recent papers have estimated the historical strength of selection for mutations conferring disease resistance. These studies are based on simple population genetic models that do not take account of factors such as spatial and family structure. Such factors may have a substantial impact on the strength of natural selection through inclusive fitness effects. That is, people have a strong tendency to live with relatives and therefore have a high probability of transmitting infectious diseases to them. Thus, an allele that protects an individual against disease infection also protects that individual's family members. Because some of these family members are likely to also be carrying the allele, selection for that allele is magnified by family structure. In this paper, I use mathematical modeling techniques to explore the impact of such kin selection on the strength of selection for infectious disease resistance alleles. I show that if the resistance allele has the same proportional effect on both within- and between-family transmission, then the impact of kin selection is relatively minor. Selection coefficients are increased by 5-35%, with a greater benefit for weaker alleles. The reason is that an individual with a strong resistance allele does not need much protection from infection by family members and thus does not benefit much from their alleles. The effect of kin selection can be dramatic, however, if the resistance allele has a larger effect on between-family transmission than within-family transmission (which can occur if between-family infection rates are much smaller than within-family rates), increasing selection coefficients by as much as two- to threefold. These results show conditions when it is important to consider family structure in estimates of the strength of selection for infectious disease resistance alleles.
 
Article
After an estimated five million years of independent evolution, the barred tiger salamander (Ambystoma tigrinum mavortium) was introduced by bait dealers into the native range of the California tiger salamander (A. californiense). Hybridization and backcrossing have been occurring in central California for 50-60 years, or an estimated 15-30 generations. We studied genetic and ecological factors influencing admixture of these two divergent gene pools by analyzing frequencies of hybrid genotypes in three kinds of breeding habitats: natural vernal pools, ephemeral man-made cattle ponds, and perennial man-made ponds. Perennial ponds tended to have higher frequencies of nonnative alleles than either type of seasonal pond, even in cases where perennial and seasonal ponds are within a few hundred meters. Thus, the hybrid zone has a mosaic structure that depends on pond hydrology or ecology. The presence of some broadly acting constraints on admixture is suggested by linkage disequilibria between physically unlinked molecular markers within ponds. In addition, we found several marker-specific deviations from Hardy-Weinberg equilibrium. One marker showed a consistent deficit of heterozygotes across pond types. Another showed heterozygote deficits only in vernal pools. A third was more likely to have heterozygote excess in ephemeral cattle ponds. These patterns indicate that admixture is influenced by complex genotype-by-environment interactions.
 
Article
Nonrandom patterns of gene dispersal have been identified as possible causes of genetic structuring within populations. Attempts to model these patterns have generally focused solely on the effects of isolation by distance, but the processes involved are more complex than such modeling suggests. Here, we extend considerations of gene dispersal processes beyond simple isolation by distance effects by directly evaluating the effects of kin-structured gene dispersal mediated by the group dispersal of related seeds within fruits (i.e., kin-structured seed dispersal) by birds on genetic structure in Ilex leucoclada, a clonal dioecious shrub. To examine the genetic structure patterns, we established two 30x30 m plots (one with immature soils in old-growth forest and one in secondary forest, designated IM and SC, respectively) with different I. leucoclada stem densities. In these two plots 145 and 510 stems were found, representing 78 and 85 genets, respectively, identified by analyzing their genotypes at eight microsatellite loci. The clonal structure was stronger in the SC plot than in the IM plot. Correlograms of coancestry for genets in both plots exhibited significant, positive, high values in the shortest distance class, indicating the presence of strong genetic structure. However, Sp statistics revealed that the pattern of the genetic structure differed between the plots. In addition, to estimate the family structure within fruits, we sampled forty fruits, in total, from 15 randomly selected plants in the area around the IM and SC plots, and found that 80% of the fruits were multiseeded and 42-100% of the multiseeded fruits contained at least one pair of full sibs. Simulations based on these estimates demonstrated that the group dispersal of related seeds produced through correlated mating both within and across fruits, but not unstructured half-sib dispersal, could generate the observed magnitude and trends of genetic structure found in the IM plot. Furthermore, in addition to kin-structured seed dispersal, isolation by distance processes is also likely to promote genetic substructuring in the SC plot. After discussing possible ecological factors that may have contributed to the observed genetic structure, we contrast our results with those predicted by general isolation by distance models, and propose that kin-structured seed dispersal should promote some evolutionary phenomena, and thus should be incorporated, where appropriate, in models of gene dispersal in natural plant populations.
 
Article
Recently, the utility of modern phylogenetic comparative methods (PCMs) has been questioned because of the seemingly restrictive assumptions required by these methods. Although most comparative analyses involve traits thought to be undergoing natural or sexual selection, most PCMs require an assumption that the traits be evolving by less directed random processes, such as Brownian motion (BM). In this study, we use computer simulation to generate data under more realistic evolutionary scenarios and consider the statistical abilities of a variety of PCMs to estimate correlation coefficients from these data. We found that correlations estimated without taking phylogeny into account were often quite poor and never substantially better than those produced by the other tested methods. In contrast, most PCMs performed quite well even when their assumptions were violated. Felsenstein's independent contrasts (FIC) method gave the best performance in many cases, even when weak constraints had been acting throughout phenotypic evolution. When strong constraints acted in opposition to variance-generating (i.e., BM) forces, however, FIC correlation coefficients were biased in the direction of those BM forces. In most cases, all other PCMs tested (phylogenetic generalized least squares, phylogenetic mixed model, spatial autoregression, and phylogenetic eigenvector regression) yielded good statistical performance, regardless of the details of the evolutionary model used to generate the data. Actual parameter estimates given by different PCMs for each dataset, however, were occasionally very different from one another, suggesting that the choice among them should depend on the types of traits and evolutionary processes being considered.
 
Article
Thirteen-year cicadas of brood XIX from northern Arkansas, Missouri, and southern Illinois (lineage A) are known to be genetically different at two marker loci (mitochondrial DNA and abdominal color) from 13-year cicadas to the south (lineage B) that emerge in the same year. Because 17-year cicadas from all broods (year classes) are indistinguishable from lineage A at these two marker loci, previous workers suggested that the lineage A cicadas of 13-year brood XIX were derived from 17-year cicadas by life-cycle switching (allochrony). Data presented here show that, over the same northern geographic range, lineage A is also present in 13-year cicadas belonging to brood XXIII (which always emerges four years later than brood XIX). Detailed sampling along the putative life-cycle-switching boundary in 13-year brood XXIII revealed a previously unsuspected broad zone of overlap where populations contained individuals of both lineages A and B. Despite this sympatry, and previous reports of a lack of behavioral barriers to interbreeding, a strong correlation between mitochondrial haplotype and abdominal color suggests that assortative mating has taken place. Lineage A 13-year cicadas from both broods XIX and XXIII are only found within a gap in the spatial distribution of 17-year cicadas. This, in combination with the lack of differentiation between lineage A 13- and 17-year cicadas at the marker loci and new behavioral data for 13-year brood XIX, suggests a recent derivation of all northern 13-year cicadas from the 17-year cicadas via life-cycle switching. We discuss the implications of these allochronic shifts for speciation.
 
Article
2 Louisiana State Arthropod Museum, LSU Agricultural Center, Louisiana State University, Baton Rouge, Louisiana 70808 E-mail: ccarlt@lsu.edu
 
Article
Genetic isolation by distance (IBD) has rarely been described in marine species with high potential for dispersal at both the larval and adult life-history stages. Here, we report significant relationships between inferred levels of gene flow and geographic distance in the Atlantic cod, Gadus morhua, at 10 nuclear restriction-fragment-length-polymorphism (RFLP) loci at small regional scales in the western north Atlantic region (< 1,600 km) that mirror those previously detected over its entire geographic range (up to 7,300 km). Highly significant allele frequency differences were observed among eight northwestern Atlantic populations, although the mean FST for all 10 loci was only 0.014. Despite this weak population structuring, the distance separating populations explained between 54% and 62% of the variation in gene flow depending on whether nine or 10 loci were used to estimate Nm. Across the species' entire geographic range, highly significant differences were observed among six regional populations at nine of the 10 loci (mean FST = 0.068) and seven loci exhibited significant negative relationships between gene flow and distance. At this large geographic scale, natural selection acting in the vicinity of one RFLP locus (GM798) had a significant effect on the correlation between gene flow and distance, and eliminating it from the analysis caused the coefficient of determination to increase from 17% to 62%. The role of vicariance was assessed by sequentially removing populations from the analysis and was found to play a minor role in contributing to the relationship between gene flow and distance at either geographic scale. The correlation between gene flow and distance detected in G. morhua at small and large spatial scales suggests that dispersal distances and effective population sizes are much smaller than predicted for the species and that the recent age of populations, rather than extensive gene flow, may be responsible for its weak population structure. Our results suggest that interpreting limited genetic differences among populations as reflecting high levels of ongoing gene flow should be made with caution.
 
Article
Species as evolutionary lineages are expected to show greater evolutionary independence from one another than are populations within species. Two measures of evolutionary independence that stem from the study of isolation-with-migration models, one reflecting the amount of gene exchange and one reflecting the time of separation, were drawn from the literature for a large number of pairs of closely related species and pairs of populations within species. Both measures, for gene flow and time, showed broadly overlapping distributions for pairs of species and for pairs of populations within species. Species on average show more time and less gene flow than populations, but the similarity of the distributions argues against there being a qualitative difference associated with species status, as compared to populations. The two measures of evolutionary independence were similarly correlated with F(ST) estimates, which in turn also showed similar distributions for species comparisons relative to population comparisons. The measures of gene flow and separation time were examined for the capacity to discriminate intraspecific differences from interspecific differences. If used together, the two measures could be used to develop an objective (in the sense of being repeatable) measure for species diagnosis.
 
Article
The potential for local adaptation between pathogens and their hosts has generated strong theoretical and empirical interest with evidence both for and against local adaptation reported for a range of systems. We use the Linum marginale-Melampsora lini plant-pathogen system and a hierarchical spatial structure to investigate patterns of local adaptation within a metapopulation characterised by epidemic dynamics and frequent extinction of pathogen populations. Based on large sample sizes and comprehensive cross-inoculation trials, our analyses demonstrate strong local adaptation by Melampsora to its host populations, with this effect being greatest at regional scales, as predicted from the broader spatial scales at which M. lini disperses relative to L. marginale. However, there was no consistent trend for more distant pathogen populations to perform more poorly. Our results further show how the coevolutionary interaction between hosts and pathogens can be influenced by local structure such that resistant hosts select for generally virulent pathogens, while susceptible hosts select for more avirulent pathogens. Empirically, local adaptation has generally been tested in two contrasting ways: (1) pathogen performance on sympatric versus allopatric hosts; and (2) sympatric versus allopatric pathogens on a given host population. In situations where no host population is more resistant or susceptible than others when averaged across pathogen populations (and likewise, no pathogen population is more virulent or avirulent than others), results from these tests should generally be congruent. We argue that this is unlikely to be the case in the metapopulation situations that predominate in natural host-pathogen interactions, thus requiring tests that control simultaneously for variation in plant and pathogen populations.
 
Article
Metabolic rate is a key aspect of organismal biology and the identification of selective factors that have led to species differences is a major goal of evolutionary physiology. We tested whether environmental characteristics and/or diet were significant predictors of interspecific variation in rodent metabolic rates. Mass-specific basal metabolic rates (BMR) and maximum metabolic rates (MMR, measured during cold exposure in a He-O2 atmosphere) were compiled from the literature. Maximum (Tmax) and minimum (Tmin) annual mean temperatures, latitude, altitude, and precipitation were obtained from field stations close to the capture sites reported for each population (N = 57). Diet and all continuous-valued traits showed statistically significant phylogenetic signal, with the exception of mass-corrected MMR and altitude. Therefore, results of phylogenetic analyses are emphasized. Body mass was not correlated with absolute latitude, but was positively correlated with precipitation in analyses with phylogenetically independent contrasts. Conventional multiple regressions that included body mass indicated that Tmax (best), Tmin, latitude, and diet were significant additional predictors of BMR. However, phylogenetic analyses indicated that latitude was the only significant predictor of mass-adjusted BMR (positive partial regression coefficient, one-tailed P = 0.0465). Conventional analyses indicated that Tmax, Tmin (best), and altitude explained significant amounts of the variation in mass-adjusted MMR. With body mass and Tmin in the model, no additional variables were significant predictors. Phylogenetic contrasts yielded similar results. Both conventional and phylogenetic analyses indicated a highly significant positive correlation between residual BMR and MMR (as has also been reported for birds), which is consistent with a key assumption of the aerobic capacity model for the evolution of vertebrate energetics (assuming that MMR and exercise-induced maximal oxygen consumption are positively functionally related). Our results support the hypothesis that variation in environmental factors leads to variation in the selective regime for metabolic rates of rodents. However, the causes of a positive association between BMR and latitude remain obscure. Moreover, an important area for future research will be experiments in all taxa are raised under common conditions to allow definitive tests of climatic adaptation in endotherm metabolic rates and to elucidate the extent of adaptive phenotypic plasticity.
 
Article
Studies on selection for faster development in Drosophila have typically focused on the trade-offs among development time, adult weight, and adult life span. Relatively less attention has been paid to the evolution of preadult life stages and behaviors in response to such selection. We have earlier reported that four laboratory populations of D. melanogaster selected for faster development and early reproduction, relative to control populations, showed considerably reduced preadult development time and survivorship, dry weight at eclosion, and larval growth rates. Here we study the larval phase of these populations in greater detail. We show here that the reduction in development time after about 50 generations of selection is due to reduced duration of the first and third larval instars and the pupal stage, whereas the duration of the second larval instar has not changed. About 90% of the preadult mortality in the selected populations is due to larval mortality. The third instar larvae, pupae, and freshly eclosed adults of the selected populations weigh significantly less than controls, and this difference appears during the third larval instar. Thereafter, percentage weight loss during the pupal stage does not differ between selected and control populations. The minimum amount of time a larva must feed to subsequently complete development is lower in the selected populations, which also exhibit a syndrome of reduced energy expenditure through reduction in larval feeding rate, larval digging and foraging activity, and pupation height. Comparison of these results with those observed earlier in populations selected for adaptation to larval crowding and faster development under a different protocol from ours reveal differences in the evolved traits that suggest that the responses to selection for faster development are greatly affected by the larval density at which selection acts and on details of the selection pressures acting on the timing of reproduction.
 
Article
Understanding the process by which hybrid incompatibility alleles become established in natural populations remains a major challenge to evolutionary biology. Previously, we discovered a two-locus Dobzhansky-Muller incompatibility that causes severe hybrid male sterility between two inbred lines of the incompletely isolated wildflower species, Mimulus guttatus and M. nasutus. An interspecific cross between these two inbred lines revealed that the M. guttatus (IM62) allele at hybrid male sterility 1 (hms1) acts dominantly in combination with recessive M. nasutus (SF5) alleles at hybrid male sterility 2 (hms2) to cause nearly complete hybrid male sterility. In this report, we extend these genetic analyses to investigate intraspecific variation for the hms1-hms2 incompatibility in natural populations of M. nasutus and M. guttatus, performing a series of interspecific crosses between individuals collected from a variety of geographic locales. Our results suggest that hms2 incompatibility alleles are common and geographically widespread within M. nasutus, but absent or rare in M. guttatus. In contrast, the hms1 locus is polymorphic within M. guttatus and the incompatibility allele appears to be extremely geographically restricted. We found evidence for the presence of the hms1 incompatibility allele in only two M. guttatus populations that exist within a few kilometers of each other. The restricted distribution of the hms1 incompatibility allele might currently limit the potential for the hms1-hms2 incompatibility to act as a species barrier between sympatric populations of M. guttatus and M. nasutus. Extensive sampling within a single M. guttatus population revealed that the hms1 locus is polymorphic and that the incompatibility allele appears to segregate at intermediate frequency, a pattern that is consistent with either genetic drift or natural selection.
 
Article
Mating systems in plants are known to be highly labile traits, with frequent transitions from outcrossing to selfing. The genetic basis for breakdown in self-incompatibility (SI) systems has been studied, but data on variation in selfing rates in species for which the molecular basis of SI is known are rare. This study surveyed such variation in Arabidopsis lyrata (Brassicaceae), which is often considered an obligately outcrossing species, to examine the causes and genetic consequences of changes in its breeding system. Based on controlled self-pollinations in the greenhouse, three populations from the Great Lakes region of North America included a minority of self-compatible (SC) individuals, while two showed larger proportions of SC individuals and all populations contained some individuals capable of setting selfed seeds. Loss of SI was not associated with particular haplotypes at the S-locus (as estimated by alleles amplified at the SRK locus, the gene controlling female specificity) and all populations contained similar numbers of SRK alleles, suggesting that some other genetic factor is responsible for modifying the SI reaction. The loss of SI has resulted in an effective shift in the mating system, as the two populations with a high frequency of SC individuals showed significantly lower microsatellite-based multilocus outcrossing rates and higher inbreeding coefficients than the other populations. Based on microsatellites, observed heterozygosities and genetic diversity were also significantly depressed in these populations. These findings provide the unique opportunity to examine in detail the consequences of mating system changes within a species with a well-characterized SI system.
 
Article
Until recently, African and European subspecies of the honeybee (Apis mellifera L.) had been geographically separated for around 10,000 years. However, human-assisted introductions have caused the mixing of large populations of African and European subspecies in South and Central America, permitting an unprecedented opportunity to study a large-scale hybridization event using molecular analyses. We obtained reference populations from Europe, Africa, and South America and used these to provide baseline information for a microsatellite and mitochondrial analysis of the process of Africanization of the bees of the Yucatan Peninsula, Mexico. The genetic structure of the Yucatecan population has changed dramatically over time. The pre-Africanized Yucatecan population (1985) comprised bees that were most similar to samples from southeastern Europe and northern and western Europe. Three years after the arrival of Africanized bees (1989), substantial paternal gene flow had occurred from feral Africanized drones into the resident European population, but maternal gene flow from the invading Africanized population into the local population was negligible. However by 1998, there was a radical shift with both African nuclear alleles (65%) and African-derived mitochondria (61%) dominating the genomes of domestic colonies. We suggest that although European mitochondria may eventually be driven to extinction in the feral population, stable introgression of European nuclear alleles has occurred.
 
Article
Nested clade phylogeographic analysis (NCPA) is a popular method for reconstructing the demographic history of spatially distributed populations from genetic data. Although some parts of the analysis are automated, there is no unique and widely followed algorithm for doing this in its entirety, beginning with the data, and ending with the inferences drawn from the data. This article describes a method that automates NCPA, thereby providing a framework for replicating analyses in an objective way. To do so, a number of decisions need to be made so that the automated implementation is representative of previous analyses. We review how the NCPA procedure has evolved since its inception and conclude that there is scope for some variability in the manual application of NCPA. We apply the automated software to three published datasets previously analyzed manually and replicate many details of the manual analyses, suggesting that the current algorithm is representative of how a typical user will perform NCPA. We simulate a large number of replicate datasets for geographically distributed, but entirely random-mating, populations. These are then analyzed using the automated NCPA algorithm. Results indicate that NCPA tends to give a high frequency of false positives. In our simulations we observe that 14% of the clades give a conclusive inference that a demographic event has occurred, and that 75% of the datasets have at least one clade that gives such an inference. This is mainly due to the generation of multiple statistics per clade, of which only one is required to be significant to apply the inference key. We survey the inferences that have been made in recent publications and show that the most commonly inferred processes (restricted gene flow with isolation by distance and contiguous range expansion) are those that are commonly inferred in our simulations. However, published datasets typically yield a richer set of inferences with NCPA than obtained in our random-mating simulations, and further testing of NCPA with models of structured populations is necessary to examine its accuracy.
 
Article
This study is devoted to assess sex ratio variation among 33 populations of the gynodioecious Beta vulgaris ssp. maritima in Brittany (France) and to explore the causes of this variation. We showed that three different CMS (cytoplasmic male sterility) cytotypes occurred in populations, but strongly differed for their frequencies and the frequency of their associated nuclear restorer alleles (which counteract the effect of CMS and restore male fertility). No correlation was found between CMS and restorer frequencies within populations, which has been previously interpreted as a result of stochasticity. However, neutral genetic variation did not indicate recent population bottlenecks in studied populations. Moreover, no significant correlation was found between female frequency or variance and current population size. Consequently, stochastic processes could not be the major cause of sex ratio variation. Alternatively, empirical estimations of the variation of females, CMS genes and nuclear restorer allele's frequencies were compared to theoretical predictions based on a frequency-dependent selection model of gynodioecy. In particular, we showed that an absence of correlation between CMS and restorer frequencies could also occur without stochasticity. The large variation of sex ratio in Beta vulgaris could thus be explained by frequency-dependent selection acting on CMS genes and restorer alleles.
 
Article
Saccharomyces cerevisiae's ability to form the prion [PSI+] may increase the rate of evolvability, defined as the rate of appearance of heritable and potentially adaptive phenotypic variants. The increase in evolvability occurs when the appearance of the prion causes read-through translation and reveals hidden variation in untranslated regions. Eventually the portion of the phenotypic variation that is adaptive loses its dependence on the revealing mechanism. The mechanism is reversible, so the restoration of normal translation termination conceals the revealed deleterious variation, leaving the yeast without a permanent handicap. Given that the ability to form [PSI+] is known to be fixed and conserved in yeast, we construct a mathematical model to calculate whether this ability is more likely to have become fixed due to chance alone or due to its evolvability characteristics. We find that evolvability is a more likely explanation, as long as environmental change makes partial read-through of stop codons adaptive at a frequency of at least once every million years.
 
Article
The sexes often differ in the reproductive trait limiting their fitness, an observation known as Bateman's principle. In many species, females are limited by their ability to produce eggs while males are limited by their ability to compete for and successfully fertilize those eggs. As well as promoting the evolution of sex-specific reproductive strategies, this difference may promote sex differences in other life-history traits due to their correlated effects. Sex differences in disease susceptibility and immune function are common. Two hypotheses based on Bateman's principle have been proposed to explain this pattern: that selection to prolong the period of egg production favors improved immune function in females, or that the expression of secondary sexual characteristics reduces immune function in males. Both hypotheses predict a relatively fixed pattern of reduced male immune function, at least in sexually mature individuals. An alternative hypothesis is that Bateman's principle does not dictate fixed patterns of reproductive investment, but favors phenotypically plastic reproductive strategies with males and females adaptively responding to variation in fitness-limiting resource availability. Under this hypothesis, neither sex is expected to possess intrinsically superior immune function, and immunological sex differences may vary in different environments. We demonstrate that sex-specific responses to experimental manipulation of fitness-limiting resources affects both the magnitude and direction of sex differences in immune function in Drosophila melanogaster. In the absence of sexual interactions and given abundant food, the immune function of adults was maximized in both sexes and there was no sex difference. Manipulation of food availability and sexual activity resulted in female-biased immune suppression when food was limited, and male-biased immune suppression when sexual activity was high and food was abundant. The immunological cost to males of increased sexual activity was found to be due in part to reduced time spent feeding. We suggest that for species similarly limited in their reproduction, phenotypic plasticity will be an important determinant of sex differences in immune function and other life-history traits.
 
Article
We consider the evolution of ecological specialization in a landscape with two discrete habitat types connected by migration, for example, a plant-insect system with two plant hosts. Using a quantitative genetic approach. we study the joint evolution of a quantitative character determining performance in each habitat together with the changes in the population density. We find that specialization on a single habitat evolves with intermediate migration rates, whereas a generalist species evolves with both very low and very large rates of movement between habitats. There is a threshold at which a small increase in the connectivity of the two habitats will result in dramatic decrease in the total population size and the nearly complete loss of use of one of the two habitats through a process of "migrational meltdown." In some situations, equilibria corresponding to a specialist and a generalist species are simultaneously stable. Analysis of our model also shows cases of hysteresis in which small transient changes in the landscape structure or accidental demographic disturbances have irreversible effects on the evolution of specialization.
 
Article
A continuous reaction norm or performance curve represents a phenotypic trait of an individual or genotype in which the trait value may vary with some continuous environmental variable. We explore patterns of genetic variation in thermal performance curves of short-term caterpillar growth rate in a population of Pieris rapae. We compare multivariate methods, which treat performance at each test temperature as a distinct trait, with function-valued methods that treat a performance curve as a continuous function. Mean growth rate increased with increasing temperatures from 8 to 35 degrees C, was highest at 35 degrees C, and declined at 40 degrees C. There was substantial and significant variation among full-sib families in their thermal performance curves. Estimates of broad-sense genetic variances and covariances showed that genetic variance in growth rate increased more than 30-fold from low (8-11 degrees C) to high (35-40 degrees C) temperatures, even after differences in mean growth rate across temperatures were removed. Growth rate at 35 and 40 degrees C was negatively correlated genetically, suggesting a genetic trade-off in growth rate at these temperatures; this trade-off may represent either a generalist-specialist trade-off and/or variation in the optimal temperature for growth. The estimated genetic variance-covariance function (G function), the function-valued analog of the variance-covariance matrix (G matrix), was quite bumpy compared with the estimated G matrix; and results of principal component analyses of the G function were difficult to interpret. The use of orthogonal polynomials as the basis functions in current function-valued estimation methods may generate artifacts when the true G function has prominent local features, such as strong negative covariances at nearby temperatures (e.g. at 35 and 40 degrees C); this may be a particular issue for thermal performance curves and other highly nonlinear reaction norms.
 
Article
Substantial evidence from the animal kingdom shows that there is a trade-off between benefits and costs associated with rapid somatic growth. One would therefore expect growth rates under natural conditions to be close to an evolutionary optimum. Nevertheless, natural selection in many salmonid species appears to be toward larger size and earlier emergence from spawning redds, indicating a potential for increased growth rate to evolve. We tested how selection for genetic variants (growth hormone transgenic coho salmon, Oncorhynchus kisutch, with more than doubled daily growth rate potential relative to wild genotypes) depended on predator timing and food abundance during the early period of life (fry stage). In artificial redds, fry of the fast-growing genotypes showed a highly significant developmental shift, emerging from gravel nests approximately two weeks sooner, but with an 18.6% reduced survival, relative to wild-genotype fry. In seminatural streams, fry of the fast-growing genotypes suffered higher predation than those of wild genotypes when predators were present at the time of fry emergence, but this difference was less pronounced when food was scarce. In streams where predators were introduced after emergence, fry survived equally well regardless of food availability. Surviving fry grew faster in habitats provided with more food, and fast-growing genotypes also grew faster than wild genotypes when predators arrived late and food was abundant. Fewer fish migrated downstream past a waterfall when food availability was high and in the presence of predators, and wild-genotype fry were more likely to migrate than fry of the fast-growing genotypes. After being returned to the experimental streams after migration, fast-growing genotypes survived equally well as those of the same genotypes that did not migrate, whereas migrating wild genotypes experienced higher mortality relative to those of the same genotypes that did not migrate. Comparisons of growth rates between siblings retained under hatchery conditions and those from habitats with the fastest growth in the experimental stream revealed that growth rates were similar for wild genotypes in both environments, whereas the fast-growing genotypes in the streams only realized 90% of their growth potential. The present study has shown that a major shift in developmental timing can alter critical early stages affecting survival and can have a significant effect on fitness. Furthermore, ecological conditions such as food abundance and predation pressure can strongly influence the potential for fast-growing variants to survive under natural conditions. The large-scale removal of many predatory species around the world may augment the evolution of increased intrinsic growth rates in some taxa.
 
Article
Reproductive isolation can evolve either as a by-product of divergent selection or through reinforcement. We used the Cape flora of South Africa, known for its high level of pollination specialization, as a model system to test the potential role of shifts in pollination system in the speciation process. Comparative analysis of 41 sister-species pairs (representing Geraniaceae, Iridaceae, and Orchidaceae) for which complete pollinator, edaphic, and distribution data are available showed that for sister species with overlapping distribution ranges, pollination system shifts are significantly associated with edaphic shifts. In contrast, there is no significant association between pollination system shifts and edaphic shifts for allopatric sister species. These results are interpreted as evidence for reinforcement.
 
Article
Wolbachia is a widespread group of intracellular bacteria commonly found in arthropods. In many insect species, Wolbachia induce a cytoplasmic mating incompatibility (CI). If different Wolbachia infections occur in the same host species, bidirectional CI is often induced. Bidirectional CI acts as a postzygotic isolation mechanism if parapatric host populations are infected with different Wolbachia strains. Therefore, it has been suggested that Wolbachia could promote speciation in their hosts. In this article we investigate theoretically whether Wolbachia-induced bidirectional CI selects for premating isolation and therefore reinforces genetic divergence between parapatric host populations. To achieve this we combined models for Wolbachia dynamics with a well-studied reinforcement model. This new model allows us to compare the effect of bidirectional CI on the evolution of female mating preferences with a situation in which postzygotic isolation is caused by nuclear genetic incompatibilities (NI). We distinguish between nuclear incompatibilities caused by two loci with epistatic interactions, and a single locus with incompatibility among heterozygotes in the diploid phase. Our main findings are: (1) bidirectional CI and single locus NI select for premating isolation with a higher speed and for a wider parameter range than epistatic NI; (2) under certain parameter values, runaway sexual selection leads to the increase of an introduced female preference allele and fixation of its preferred male trait allele in both populations, whereas under others it leads to divergence in the two populations in preference and trait alleles; and (3) bidirectional CI and single locus NI can stably persist up to migration rates that are two times higher than seen for epistatic NI. The latter finding is important because the speed with which mutants at the preference locus spread increases exponentially with the migration rate. In summary, our results show that bidirectional CI selects for rapid premating isolation and so generally support the view that Wolbachia can promote speciation in their hosts.
 
Article
Chaotic genetic patchiness denotes unexpected patterns of genetic differentiation that are observed at a fine scale and are not stable in time. These patterns have been described in marine species with free-living larvae, but are unexpected because they occur at a scale below the dispersal range of pelagic larvae. At the scale where most larvae are immigrants, theory predicts spatially homogeneous, temporally stable genetic variation. Empirical studies have suggested that genetic drift interacts with complex dispersal patterns to create chaotic genetic patchiness. Here we use a coancestry model and individual-based simulations to test this idea. We found that chaotic genetic patterns (qualified by global FST and spatio-temporal variation in FST 's between pairs of samples) arise from the combined effects of (1) genetic drift created by the small local effective population sizes of the sessile phase and variance in contribution among breeding groups and (2) collective dispersal of related individuals in the larval phase. Simulations show that patchiness levels qualitatively comparable to empirical results can be produced by a combination of strong variance in reproductive success and mild collective dispersal. These results call for empirical studies of the effective number of breeders producing larval cohorts, and population genetics at the larval stage.
 
Article
Ecological studies suggest that hummingbird-pollinated plants in North America mimic each other to increase visitation by birds. Published quantitative trait locus (QTL) data for two Mimulus species indicate that floral traits associated with hummingbird versus bee pollination results from a few loci with major effects on morphology, as predicted by classical models for the evolution of mimicry. Thus, the architecture of genetic divergence associated with speciation may depend on the ecological context.
 
Article
The species and races of the shrews of the Sorex araneus group exhibit a broad range of chromosomal polymorphisms. European taxa of this group are parapatric and form contact or hybrid zones that span an extraordinary variety of situations, ranging from absolute genetic isolation to almost free gene flow. This variety seems to depend for a large part on the chromosome composition of populations, which are primarily differentiated by various Robertsonian fusions of a subset of acrocentric chromosomes. Previous studies suggested that chromosomal rearrangements play a causative role in the speciation process. In such models, gene flow should be more restricted for markers on chromosomes involved in rearrangements than on chromosomes common in both parent species. In the present study, we address the possibility of such differential gene flow in the context of two genetically very similar but karyotypically different hybrid zones between species of the S. araneus group using microsatellite loci mapped to the chromosome arm level. Interspecific genetic structure across rearranged chromosomes was in general larger than across common chromosomes. However, the difference between the two classes of chromosomes was only significant in the hybrid zone where the complexity of hybrids is expected to be larger. These differences did not distinguish populations within species. Therefore, the rearranged chromosomes appear to affect the reproductive barrier between karyotypic species, although the strength of this effect depends on the complexity of the hybrids produced.
 
Article
It is generally well understood that some ecological factors select for increased and others for decreased dispersal. However, it has remained difficult to assess how the evolutionary dynamics are influenced by the spatio-temporal structure of the environment. We address this question with an individual-based model that enables habitat structure to be controlled through variables such as patch size, patch turnover rate, and patch quality. Increasing patch size at the expense of patch density can select for more or less dispersal, depending on the initial configuration. In landscapes consisting of high-quality and long-lived habitat patches, patch degradation selects for increased dispersal, yet patch loss may select for reduced dispersal. These trends do not depend on the component of life-history that is affected by habitat quality or the component of life-history through which density-dependence operates. Our results are based on a mathematical method that enables derivation of both the evolutionary stable strategy and the stationary genotype distribution that evolves in a polymorphic population. The two approaches generally lead to similar predictions. However, the evolutionary stable strategy assumes that the ecological and evolutionary time scales can be separated, and we find that violation of this assumption can critically alter the evolutionary outcome.
 
Article
The thermoregulatory hypothesis proposes that endothermy in mammals and birds evolved as a thermoregulatory mechanism per se and that natural selection operated directly to increase body temperature and thermal stability through increments in resting metabolic rate. We experimentally tested this hypothesis by measuring the thermoregulatory consequences of increased metabolic rate in resting lizards (Varanus exanthematicus). A large metabolic increment was induced by feeding the animals and consequent changes in metabolic rate and body temperature were monitored. Although metabolic rate tripled at 32 degrees C and quadrupled at 35 degrees C, body temperature rose only about 0.5 degrees C. The rate of decline of body temperature in a colder environment did not decrease as metabolic rate increased. Thus, increasing the visceral metabolic rate of this ectothermic lizard established neither consequential endothermy nor homeothermy. These results are inconsistent with a thermoregulatory explanation for the evolution of endothermy.
 
Article
Ecological divergence may result when populations experience different selection regimes, but there is considerable discussion about the role of migration at the beginning stages of divergence before reproductive isolating mechanisms have evolved. However, detection of past migration is difficult in current populations and tools to differentiate genetic similarities due to migration versus recent common ancestry are only recently available. Using past volcanic eruption times as a framework, we combine morphological analyses of traits important to reproduction with a coalescent-based genetic analysis of two proximate sockeye salmon (Oncorhynchus nerka) populations. We find that this is the most recent (approximately 500 years, 100 generations) natural ecological divergence recorded in a fish species, and report that this divergence is occurring despite migration. Although studies of fish divergence following the retreat of glaciers (10,000-15,000 years ago) have contributed extensively to our understanding of speciation, the Aniakchak system of sockeye salmon provides a rare example of the initial stages of ecological divergence following natural colonization. Our results show that even in the face of continued migration, populations may diverge in the absence of a physical barrier.
 
Nest analyses of variance for male body size (pronotum length), ejaculate characteristics, and testes mass. 
Article
Ejaculates function as an integrated unit to ensure male fertility and paternity, can have a complex structure, and can experience multiple episodes of selection. Current studies on the evolution of ejaculates typically focus on phenotypic variation in sperm number, size, or related traits such as testes size as adaptations to postcopulatory male-male competition. However, the evolution of the integrated nature of ejaculate structure and function depends on genetic variation in and covariation between the component parts. Here we report a quantitative genetic study of the components of the ejaculate of the cockroach Nauphoeta cinerea, including those we know to experience postcopulatory sexual selection, in the context of functional integration of ejaculate characters. We use the patterns of genetic variation and covariation to infer how the integration of the functions of the ejaculate constrain and shape its evolution. Ejaculate components were highly variable, showed significant additive genetic variance, and moderate to high evolvability. The level of genetic variation in these characters, despite strong directional or truncating selection, may reflect the integration of multiple episodes of selection that occur in N. cinerea. There were few significant phenotypic correlations, but all the genetic correlations among ejaculate characters were significantly different from zero. The patterns of genetic variation and covariation suggest that there are important trade-offs among individual traits of the ejaculate and that evolution of ejaculate characteristics will not proceed unconstrained. Fully describing the genetic relationships among traits that perform as an integrated unit helps us understand how functional relationships constrain or facilitate the evolution of the complex structure that is the ejaculate.
 
Dimensions of 1st-laid (A), 2nd-laid (B) and 3rd-laid (C) eggs (length and breadth in mm; volume and volume difference in cm 3 ) of pairs in Gray's harbor. Sample size for each habitat type (sand/vegetated) in brackets. Data presented as mean SD. Mann-Whitney U- values shown in braces for tests where data were not normally distributed.
Article
There has been considerable debate in the study of hybrid zones as to whether hybrids may be superior to parental types within the area of contact (bounded hybrid superiority). In birds, naturally occurring hybridization is relatively common, and hybridization within this group always involves mate choice. If hybrids are superior, females choosing heterospecific mates should be expected to show higher fitness under the conditions prevalent in the hybrid zone. Hybrid superiority under these circumstances would reduce reinforcement and thereby help to maintain the hybrid zone. To examine this issue, we studied reproductive performances of hybrids and parental species of gulls (Larus occidentalis and Larus glaucescens) at two colonies within a linear hybrid zone along the west coast of the United States. This hybrid zone contains predominantly gulls of intermediate phenotype. Previous studies indicated that hybrids were superior to one or both parental types, but provided no data on possible mechanisms that underlie this hybrid superiority. Using a hybrid index designed specifically for these species, we identified to phenotype more than 300 individuals associated with nests, including both individual males and females within 73 pairs in the central portion of the hybrid zone and 74 pairs in the northern portion of the hybrid zone. There was little evidence of assortative mating, and what little there was resulted solely because of pairings within intergrades. In the central hybrid zone, females paired with hybrid males produced larger clutches and hatched and fledged more chicks compared with females paired to western gull males. This was a result of heavy predation on eggs in sand habitat, where male western gulls established territories. In contrast, many hybrid males established territories in vegetated cover that was less vulnerable to predation. In the northern part of the hybrid zone, clutch size did not differ among pair categories, however, there were differences in hatching and fledging success, with females paired to hybrid males showing better success compared to females paired to glaucous-winged gull males. Hybrids showed better hatching and fledging success in the north because hybrids are more like western gulls than glaucous-winged gulls in foraging behavior, taking a higher percentage of fish in their diet, which enhances chick growth and survival. This is believed to be the first documentation of bounded hybrid superiority that delineates the mechanisms that underlie hybrid superiority.
 
Article
Animal color pattern phenotypes evolve rapidly. What influences their evolution? Because color patterns are used in communication, selection for signal efficacy, relative to the intended receiver's visual system, may explain and predict the direction of evolution. We investigated this in bowerbirds, whose color patterns consist of plumage, bower structure, and ornaments and whose visual displays are presented under predictable visual conditions. We used data on avian vision, environmental conditions, color pattern properties, and an estimate of the bowerbird phylogeny to test hypotheses about evolutionary effects of visual processing. Different components of the color pattern evolve differently. Plumage sexual dimorphism increased and then decreased, while overall (plumage plus bower) visual contrast increased. The use of bowers allows relative crypsis of the bird but increased efficacy of the signal as a whole. Ornaments do not elaborate existing plumage features but instead are innovations (new color schemes) that increase signal efficacy. Isolation between species could be facilitated by plumage but not ornaments, because we observed character displacement only in plumage. Bowerbird color pattern evolution is at least partially predictable from the function of the visual system and from knowledge of different functions of different components of the color patterns. This provides clues to how more constrained visual signaling systems may evolve.
 
Article
Mate choice based on sexual ornaments can impose strong selection, which raises the question of how genetic variation in ornaments is maintained. One mechanism that has been proposed is genic capture. If ornament expression is influenced by general condition and condition is under polygenic control, selection will be inefficient in removing genetic variation. Here we analyze whether the genetic architecture of beak color in a population of zebra finches supports this hypothesis. Zebra finch beak color is commonly assumed to be under strong selection by mate choice, although some of the evidence is ambiguous. We show that beak redness has a heritability of 34% in our population and that it is strongly genetically correlated between the sexes, suggesting that it is largely controlled by the same genes in males and females. We mapped variation in beak redness based on 1404 single-nucleotide polymorphism (SNP) markers genotyped in a large pedigree. We find evidence for linkage on four chromosomes (Tgu1, Tgu5, Tgu13, Tgu21), which together explain a large part of the additive genetic variance. Our finding of genomic regions with major additive effects is not consistent with directional selection and genic capture, but rather suggests a role of antagonistic pleiotropy in maintaining genetic variation.
 
Article
The ability of populations to undergo adaptive evolution depends on the presence of genetic variation for ecologically important traits. The maintenance of genetic variation may be influenced by many variables, particularly long-term effective population size and the strength and form of selection. The roles of these factors are controversial and there is very little information on their impacts for quantitative characters. The aims of this study were to determine the impacts of population size and variable versus constant prior environmental conditions on fitness and the magnitude of response to selection. Outbred and inbred populations of Drosophila melanogaster were maintained under benign, constant stressful, and variably stressful conditions for seven generations, and then forced to adapt to a novel stress for seven generations. Fitness and adaptability were assayed in each replicate population. Our findings are that: (1) populations inbred in a variable environment were more adaptable than those inbred in a constant environment; (2) populations adapted to a prior stressful environment had greater fitness when reared in a novel stress than those less adapted to stress; (3) inbred populations had lower fitness and were less adaptable than the outbred population they were derived from; and (4) strong lineage effects were detectable across environments in the inbred populations.
 
Top-cited authors
Bruce Weir
  • University of Washington Seattle
Stevan James Arnold
  • Oregon State University
Wayne Maddison
  • University of British Columbia - Vancouver
David Maddison
  • Oregon State University
Michael Wade
  • Indiana University Bloomington