The importance of contingency versus predictability in evolution has been a long-standing issue, particularly the interaction between genetic background, founder effects, and selection. Here we address experimentally the effects of genetic background and founder events on the repeatability of laboratory adaptation in Drosophila subobscura populations for several functional traits. We found disparate starting points for adaptation among laboratory populations derived from independently sampled wild populations for all traits. With respect to the subsequent evolutionary rate during laboratory adaptation, starvation resistance varied considerably among foundations such that the outcome of laboratory evolution is rather unpredictable for this particular trait, even in direction. In contrast, the laboratory evolution of traits closely related to fitness was less contingent on the circumstances of foundation. These findings suggest that the initial laboratory evolution of weakly selected characters may be unpredictable, even when the key adaptations under evolutionary domestication are predictable with respect to their trajectories.

Coevolutionary interactions are thought to play a crucial role in diversification of hosts and parasitoids. Furthermore, resource availability has been shown to be a fundamental driver of species diversity. Yet, we still do not have a clear understanding of how resource availability mediates the diversity generated by coevolution between hosts and parasitoids over time. We used experiments with bacteria and bacteriophage to test how resources affect variation in the competitive ability of resistant hosts and temporal patterns of diversity in the host and parasitoid as a result of antagonistic coevolution. Bacteria and bacteriophage coevolved for over 150 bacterial generations under high and low-resource conditions. We measured relative competitive ability of the resistant hosts and phenotypic diversity of hosts and parasitoids after the initial invasion of resistant mutants and again at the end of the experiment. Variation in relative competitive ability of the hosts was both time- and environment-dependent. The diversity of resistant hosts, and the abundance of host-range mutants attacking these phenotypes, differed among environments and changed over time, but the direction of these changes differed between the host and parasitoid. Our results demonstrate that patterns of fitness and diversity resulting from coevolutionary interactions can be highly dynamic.

Sterility barriers, ranging from incomplete to fully developed, were recently demonstrated within taxonomic species of the genus Draba, suggesting the existence of numerous, cryptic biological species. Because these taxa are predominately selfers and of Pleistocene origin, it was concluded that hybrid sterility evolved quickly and possibly by genetic drift. Here we used genetic mapping and QTL analyses to determine the genetic basis of hybrid sterility between geographically distant populations of one of these taxonomic species, Draba nivalis. Fifty microsatellite loci were mapped, and QTL analyses identified five loci underlying seed fertility and two underlying pollen fertility. Four of five seed fertility QTLs reduced fertility in heterozygotes, an observation most consistent with drift-based fixation of underdominant sterility loci. However, several nuclear–nuclear interactions were also found, including two that acted like reciprocal translocations with lowest fitness in double heterozygotes, and two that had a pattern of fitness consistent with Bateson–Dobzhansky–Muller incompatibilities. In contrast, pollen fertility QTLs exhibited additive inheritance, with lowest fertility associated with the paternal allele, a pattern of inheritance suggestive of cytonuclear incompatibilities. The results imply that multiple genetic mechanisms underlie the rapid evolution of reproductive barriers in Draba.

Geographically structured genetic variants provide an effective means to assess sources of natural selection and mechanisms of adaptation to local environments. Correlated selection pressures along environmental gradients favor subdivision of genomes through chromosomal rearrangement. This study examines populations of Drosophila americana to evaluate selection pressures affecting chromosomal forms distinguished by a centromeric fusion. Analyses of chromosomal polymorphism throughout the Mississippi River Valley in the central United States reveal the presence of a distinct latitudinal cline for the chromosomal rearrangement. The cline has a width of 623 km centered at 35.97°N and displays a characteristic sigmoid shape consistent with a balance between selection and dispersal. Extreme low temperature during January, an indicator of winter severity, was identified as the environmental variable that most accurately predicts arrangement frequency. An intriguing relationship identified between the chromosomal cline and operational sex ratio indicates that these alternative arrangements of the X chromosome may influence sex-specific survival. A hypothesis for the cline is presented wherein variation associated with the alternative chromosome forms influences distinct overwintering strategies. The resulting subdivision within the genome embodies a transitory stage of a speciation process in which locally adapted gene complexes provide a foundation for species formation.

A common pattern in time-calibrated molecular phylogenies is a signal of rapid diversification early in the history of a radiation. Because the net rate of diversification is the difference between speciation and extinction rates, such “explosive-early” diversification could result either from temporally declining speciation rates or from increasing extinction rates through time. Distinguishing between these alternatives is challenging but important, because these processes likely result from different ecological drivers of diversification. Here we develop a method for estimating speciation and extinction rates that vary continuously through time. By applying this approach to real phylogenies with explosive-early diversification and by modeling features of lineage-accumulation curves under both declining speciation and increasing extinction scenarios, we show that a signal of explosive-early diversification in phylogenies of extant taxa cannot result from increasing extinction and can only be explained by temporally declining speciation rates. Moreover, whenever extinction rates are high, “explosive early” patterns become unobservable, because high extinction quickly erases the signature of even large declines in speciation rates. Although extinction may obscure patterns of evolutionary diversification, these results show that decreasing speciation is often distinguishable from increasing extinction in the numerous molecular phylogenies of radiations that retain a preponderance of early lineages.

More than 80% of Madagascar's 12,000 plant species are endemic with the degree of endemism reaching as much as 95% in the scaly tree ferns, an important species rich component of Madagascar's evergreen rainforests. Predominantly African or Asian ancestry and divergence times usually postdating the separation of Madagascar from the Gondwanan landmasses have been demonstrated for several Madagascan animal and angiosperm groups. However, evolutionary studies of rainforest-specific lineages are scarce and the ecological context of radiation events has rarely been investigated. Here, we examine the evolution of Madagascan tree ferns as a rainforest-specific model family, integrate results from bioclimatic niche analysis with a dated phylogenetic framework, and propose an evolutionary scenario casting new light on our knowledge of the evolution of large island endemic clades. We show that Madagascar's extant tree fern diversity springs from three distinct ancestors independently colonizing Madagascar in the Miocene and that these three monophyletic clades diversified in three coincident radiation bursts during the Pliocene, reaching exceptionally high diversification rates and most likely responding to a common climatic trigger. Recent diversification bursts may thus have played a major role in the evolution of the extant Madagascan rainforest biome, which hence contains a significant number of young, neoendemic taxa.

Cophyline narrow-mouthed frogs (Anura: Microhylidae) are a diverse endemic radiation of Madagascar. Cophylines contain a high proportion of range restricted species and constitute a good model system to understand patterns of evolutionary diversification in tropical ecosystems. We combine spatial and phylogenetic analyses for a near-complete taxon sample to test competing explanations for patterns of species richness (SR) and endemism. Our reconstruction of the phylogeny of cophylines indicates the presence of 22 new species and several instances of nonmonophyly. We found a strong historical signal in current cophyline ranges indicating a high degree of spatial niche conservatism in clade diversification, with clades occurring in the North of Madagascar constituting the most derived in the phylogeny. We identified six positively correlated centers of SR and endemism that can neither be explained by stochastic models such as elevational or latitudinal mid-domain effect, nor by low-elevation river catchments. Instead, the locations of these centers in areas spanning a high altitudinal range in combination with specific climatic parameters support a key role of mountainous areas for speciation of these anurans, although we cannot exclude an influence of habitat loss due to human impact. High conservation priority is ascribed to these areas.

Despite hundreds of reports involving both plants and animals, the mechanisms underlying introgression remain obscure, even if some form of selection is frequently invoked. Introgression has repeatedly been reported in species that have recently colonized a new habitat, suggesting that demographic processes should be given more attention for understanding the mechanisms of introgression. Here we show by spatially explicit simulations that massive introgression of neutral genes takes place during the invasion of an occupied territory if interbreeding is not severely prevented between the invading and the local species. We also demonstrate that introgression occurs almost exclusively from the local to the invading species, especially for populations located far away from the source of the invasion, and this irrespective of the relative densities of the two species. This pattern is strongest at markers experiencing reduced gene flow, in keeping with the observation that organelle genes are often preferentially introgressed across species boundaries. A survey of the literature shows that a majority of published empirical studies of introgression during range expansions, in animals and in plants, follow the predictions of our model. Our results imply that speciation genes can be identified by comparing genomes of interfertile native and invading species pairs.

Sex allocation theory has proved extremely successful at predicting when individuals should adjust the sex of their offspring in response to environmental conditions. However, we know rather little about the underlying genetics of sex ratio or how genetic architecture might constrain adaptive sex-ratio behavior. We examined how mutation influenced genetic variation in the sex ratios produced by the parasitoid wasp Nasonia vitripennis. In a mutation accumulation experiment, we determined the mutability of sex ratio, and compared this with the amount of genetic variation observed in natural populations. We found that the mutability (h²_m) ranges from 0.001 to 0.002, similar to estimates for life-history traits in other organisms. These estimates suggest one mutation every 5–60 generations, which shift the sex ratio by approximately 0.01 (proportion males). In this and other studies, the genetic variation in N. vitripennis sex ratio ranged from 0.02 to 0.17 (broad-sense heritability, H²). If sex ratio is maintained by mutation–selection balance, a higher genetic variance would be expected given our mutational parameters. Instead, the observed genetic variance perhaps suggests additional selection against sex-ratio mutations with deleterious effects on other fitness traits as well as sex ratio (i.e., pleiotropy), as has been argued to be the case more generally.

Hybridization between distinct species may lead to introgression of genes across species boundaries, and this pattern can potentially persist for extended periods as long as selection at some loci or genomic regions prevents thorough mixing of gene pools. However, very few reliable estimates of long-term levels of effective migration are available between hybridizing species throughout their history. Accurate estimates of divergence dates and levels of gene flow require data from multiple unlinked loci as well as an analytical framework that can distinguish between lineage sorting and gene flow and incorporate the effects of demographic changes within each species. Here we use sequence data from 18 anonymous nuclear loci in two broadly sympatric sunflower species, Helianthus annuus and H. petiolaris, analyzed within an “isolation with migration” framework to make genome-wide estimates of the ages of these two species, long-term rates of gene flow between them, and effective population sizes and historical patterns of population growth. Our results indicate that H. annuus and H. petiolaris are approximately one million years old and have exchanged genes at a surprisingly high rate (long-term N_efm estimates of approximately 0.5 in each direction), with somewhat higher rates of introgression from H. annuus into H. petiolaris than vice versa. In addition, each species has undergone dramatic population expansion since divergence, and both species have among the highest levels of genetic diversity reported for flowering plants. Our results provide the most comprehensive estimate to date of long-term patterns of gene flow and historical demography in a nonmodel plant system, and they indicate that species integrity can be maintained even in the face of extensive gene flow over a prolonged period.

Divergent selection on traits involved in both local adaptation and the production of mating signals can strongly facilitate population differentiation. Because of its links to foraging morphologies and cultural inheritance song of birds can contribute particularly strongly to maintenance of local adaptations. In two adjacent habitats—native Sonoran desert and urban areas—house finches (Carpodacus mexicanus) forage on seeds that are highly distinct in size and shell hardness and require different bite forces and bill morphologies. Here, we first document strong and habitat-specific natural selection on bill traits linked to bite force and find adaptive modifications of bite force and bill morphology and associated divergence in courtship song between the two habitats. Second, we investigate the developmental basis of this divergence and find that early ontogenetic tissue transformation in bill, but not skeletal traits, is accelerated in the urban population and that the mandibular primordia of the large-beaked urban finches express bone morphogenetic proteins (BMP) earlier and at higher level than those of the desert finches. Further, we show that despite being geographically adjacent, urban and desert populations are nevertheless genetically distinct corroborating findings of early developmental divergence between them. Taken together, these results suggest that divergent selection on function and development of traits involved in production of mating signals, in combination with localized learning of such signals, can be very effective at maintaining local adaptations, even at small spatial scales and in highly mobile animals.

Most phylogenetic comparative methods used for testing adaptive hypotheses make evolutionary assumptions that are not compatible with evolution toward an optimal state. As a consequence they do not correct for maladaptation. The “evolutionary regression” that is returned is more shallow than the optimal relationship between the trait and environment. We show how both evolutionary and optimal regressions, as well as phylogenetic inertia, can be estimated jointly by a comparative method built around an Ornstein–Uhlenbeck model of adaptive evolution. The method considers a single trait adapting to an optimum that is influenced by one or more continuous, randomly changing predictor variables.

Leaf shape is one of the most variable plant traits. Previous work has provided much indirect evidence that leaf-shape variation is adaptive and that leaf shape influences thermoregulation, water balance, and resistance to natural enemies. Nevertheless, there is little direct evidence that leaf shape actually affects plant fitness. In this study, we first demonstrate that populations of the ivyleaf morning glory, Ipomoea hederacea, in North and South Carolina are frequently polymorphic at a locus that influences leaf shape. We then employ several field experiments to show that this polymorphism is subject to selection. In two of the experiments, at different sites, heterozygotes enjoyed a fitness advantage over both homozygotes. At a third site, in one year directional selection favored lobed leaves, whereas in a second year the pattern of fitnesses was consistent with similar directional selection or heterozygote superiority. Computer simulations of heterozygote advantage under the high selfing rates of I. hederacea indicate that balancing selection of the magnitude observed can by itself stabilize the polymorphism, although spatially and temporally variable selection may also contribute to its long-term maintenance.

Mate-choice imprinting, the determination of mating preferences at an early age based on an individual's observation of adults, plays a role in mate choice in a wide variety of animals. Theoretical work has thus far been focused either on the effects of mate-choice imprinting on the evolution of the male trait used as a mating cue, or on the evolution of imprinting against a nonimprinting background. We ask the question: if multiple types of imprinting are possible in a species, which is likely to evolve? We develop a haploid population genetic model to compare the evolution of three forms of imprinting: paternal, maternal, and oblique (nonparental adult) imprinting. We find that paternal imprinting is the most likely to evolve, whereas maternal and oblique are nearly equivalent. We identify two factors that determine a strategy's success: its “imprinting set,” the set of individuals imprinted upon, and phenogenotypic disequilibrium, the association between imprinted preferences and mating cues. We assess the predictive power of these factors, and find that the imprinting set is the primary determinant of a strategy's success. We suggest that the imprinting set concept may be generalized to predict the success of additional imprinting strategies, such as mate-choice copying.

Animals of many species accept or solicit recurring copulations with the same partner; i.e., show repeated mating. An evolutionary explanation for this excess requires that the advantages of repeated mating outweigh the costs, and that behavioral components of repeated mating are genetically influenced. There can be benefits of repeated mating for males when there is competition for fertilizations or where the opportunities for inseminating additional mates are rare or unpredictable. The benefits to females are less obvious and, depending on underlying genetic architecture, repeated mating may have evolved as a correlated response to selection on males. We investigated the evolution of repeated mating with the same partner in the burying beetle Nicrophorus vespilloides by estimating the direct and indirect fitness benefits for females and the genetics of behavior underlying repeated mating. The number of times a female mated had minimal direct and no indirect fitness benefits for females. The behavioral components of repeated mating (mating frequency and mating speed) were moderately negatively genetically correlated in males and uncorrelated in females. However, mating frequency and mating speed were strongly positively genetically correlated between males and females. Our data suggest that repeated mating by female N. vespilloides may have evolved as a correlated response to selection on male behavior rather than in response to benefits of repeated mating for females.

Despite a massive research effort, our understanding of why, in most vertebrates, males compete for mates and females care for offspring remains incomplete. Two alternative hypotheses have been proposed to explain the direction of causality between parental care and sexual selection. Traditionally, sexual selection has been explained as a consequence of relative parental investment, where the sex investing less will compete for the sex investing more. However, a more recent model suggests that parental care patterns result from sexual selection acting on one sex favoring mating competition and lower parental investment. Using species-level comparative analyses on Tanganyikan cichlid fishes we tested these alternative hypotheses employing a proxy of sexual selection based on mating system, sexual dichromatism, and dimorphism data. First, while controlling for female reproductive investment, we found that species with intense sexual selection were associated with female-only care whereas species with moderate sexual selection were associated with biparental care. Second, using contingency analyses, we found that, contrary to the traditional view, evolutionary changes in parental care type are dependent on the intensity of sexual selection. Hence, our results support the hypothesis that sexual selection determines parental care patterns in Tanganyikan cichlid fishes.

Postcranial ossification sequences in 24 therian mammals and three outgroup taxa were obtained using clear staining and computed tomography to test the hypothesis that the marsupial forelimb is developmentally accelerated, and to assess patterns of therian postcranial ossification. Sequence rank variation of individual bones, phylogenetic analysis, and algorithm-based heterochrony optimization using event pairs were employed. Phylogenetic analysis only recovers Marsupialia, Australidelphia, and Eulipotyphla. Little heterochrony is found within marsupials and placentals. However, heterochrony was observed between marsupials and placentals, relating to late ossification in hind limb long bones and early ossification of the anterior axial skeleton. Also, ossification rank position of marsupial forelimb and shoulder girdle elements is more conservative than that of placentals; in placentals the hind limb area is more conservative. The differing ossification patterns in marsupials can be explained with a combination of muscular strain and energy allocation constraints, both resulting from the requirement of active movement of the altricial marsupial neonates toward the teat. Peramelemorphs, which are comparatively passive at birth and include species with relatively derived forelimbs, differ little from other marsupials in ossification sequence. This suggests that ossification heterochrony in marsupials is not directly related to diversity constraints on the marsupial forelimb and shoulder girdle.

An important challenge in evolutionary biology is to understand how major changes in body form arise. The dramatic transition from a lizard-like to snake-like body form in squamate reptiles offers an exciting system for such research because this change is replicated dozens of times. Here, we use morphometric data for 258 species and a time-calibrated phylogeny to explore rates and patterns of body-form evolution across squamates. We also demonstrate how time-calibrated phylogenies may be used to make inferences about the time frame over which major morphological transitions occur. Using the morphometric data, we find that the transition from lizard-like to snake-like body form involves concerted evolution of limb reduction, digit loss, and body elongation. These correlations are similar across squamate clades, despite very different ecologies and >180 million years (My) of divergence. Using the time-calibrated phylogeny and ancestral reconstructions, we find that the dramatic transition between these body forms can occur in 20 My or less, but that seemingly intermediate morphologies can also persist for tens of millions of years. Finally, although loss of digits is common, we find statistically significant support for at least six examples of the re-evolution of lost digits in the forelimb and hind limb.

Flightlessness in insects is generally thought to have evolved due to changes in habitat environment or habitat isolation. Loss of flight may have changed reproductive traits in insects, but very few attempts have been made to assess evolutionary relationships between flight and reproductive traits in a group of related species. We elucidated the evolutionary history of flight loss and its relationship to evolution in food habit, relative reproductive investment, and egg size in the Silphinae (Coleoptera: Silphidae). Most flight-capable species in this group feed primarily on vertebrate carcasses, whereas flightless or flight-dimorphic species feed primarily on soil invertebrates. Ancestral state reconstruction based on our newly constructed molecular phylogenetic tree implied that flight muscle degeneration occurred twice in association with food habit changes from necrophagy to predatory, suggesting that flight loss could evolve independently from changes in the environmental circumstances per se. We found that total egg production increased with flight loss. We also found that egg size increased with decreased egg number following food habit changes in the lineage leading to predaceous species, suggesting that selection for larger larvae intensified with the food habit change. This correlated evolution has shaped diverse life-history patterns among extant species of Silphinae.

Several techniques, such as concatenation and consensus methods, are available for combining data from multiple loci to produce a single statement of phylogenetic relationships. However, when multiple alleles are sampled from individual species, it becomes more challenging to estimate relationships at the level of species, either because concatenation becomes inappropriate due to conflicts among individual gene trees, or because the species from which multiple alleles have been sampled may not form monophyletic groups in the estimated tree. We propose a Bayesian hierarchical model to reconstruct species trees from multipleallele, multilocus sequence data, building on a recently proposed method for estimating species trees from single allele multilocus data. A two-step Markov Chain Monte Carlo (MCMC) algorithm is adopted to estimate the posterior distribution of the species tree. The model is applied to estimate the posterior distribution of species trees for two multiple-allele datasets—yeast (Saccharomyces) and birds (Manacus—manakins). The estimates of the species trees using our method are consistent with those inferred from other methods and genetic markers, but in contrast to other species tree methods, it provides credible regions for the species tree. The Bayesian approach described here provides a powerful framework for statistical testing and integration of population genetics and phylogenetics.

Cope's Rule states that the size of species tends to increase along an evolutionary lineage. A basic statistical framework is elucidated for testing Cope's Rule and some surprising complications are pointed out. If Cope's Rule is formulated in terms of mean size, then it is not invariant to the way in which size is measured. If Cope's Rule is formulated in terms of median size, then it is not invariant to the degree of separation between ancestral and descendant species. Some practical problems in assessing Cope's Rule are also described. These results have implications for the empirical assessment of Cope's Rule.

In most female mammals, one of the two X chromosomes is inactivated early in embryogenesis. Expression of most genes on this chromosome is shut down, and the inactive state is maintained throughout life in all somatic cells. It is generally believed that X-inactivation evolved as a means of achieving equal gene expression in males and females (dosage compensation). Following degeneration of genes on the Y chromosome, gene expression on X chromosomes in males and females is upregulated. This results in closer to optimal gene expression in males, but deleterious overexpression in females. In response, selection is proposed to favor inactivation of one of the X chromosomes in females, restoring optimal gene expression. Here, we make a first attempt at shedding light on this intricate process from a population genetic perspective, elucidating the sexually antagonistic selective forces involved. We derive conditions for the process to work and analyze evolutionary stability of the system. The implications of our results are discussed in the light of empirical findings and a recently proposed alternative hypothesis for the evolution of X-inactivation.

A stochastic computer simulation model was created to compare the combined effects of selection and genetic drift on the dynamics of S-alleles under full sporophytic self-incompatibility (SI) versus transient SI, a form of partial SI in which flowers become self-compatible as they age. S-alleles were lost more rapidly with transient than with full SI, as is expected with weakened frequency-dependent selection. Based on these results, equilibrium S-allele diversity is expected to be lower with partial SI for populations of comparable size and migration rates. Consistent with model results, a comparison of the proportion of incompatible crosses in full diallel experiments for a fully SI and a transiently SI species in the annual genus Leptosiphon suggests that S-allele diversity is lower in the partially SI species. Results of the simulation model indicate that the transmission advantage of self-fertilization can have complex effects on S-allele dynamics in partial SI systems.

Understanding the biological conditions and the genetic basis of early stages of sexual isolation and speciation is an outstanding question in evolutionary biology. It is unclear how much genetic and phenotypic variation for mating preferences and their phenotypic cues is segregating within widespread and human-commensal species in nature. A recent case of incipient sexual isolation between Zimbabwe and cosmopolitan populations of the human-commensal fruit fly Drosophila melanogaster indicates that such species may initiate the process of sexual isolation. However, it is still unknown whether other geographical populations have undergone evolution of mating preferences. In this study we present new data on multiple-choice mating tests revealing partial sexual isolation between the United States and Caribbean populations. We relate our findings to African populations, showing that Caribbean flies are partially sexually isolated from Zimbabwe flies, but mate randomly with West African flies, which also show partial sexual isolation from the United States and Zimbabwe flies. Thus, Caribbean and West African populations seem to exhibit distinct mating preferences relative to populations in the United States and in Zimbabwe. These results suggest that widespread and human-commensal species may harbor different types of mating preferences across their geographical ranges.

Many multicellular organisms have evolved a dedicated germline. This can benefit the whole organism, but its advantages to genetic parasites have not been explored. Here I model the evolutionary success of a selfish element, such as a transposable element or endosymbiont, which is capable of creating or strengthening a germline-soma distinction in a primitively multicellular host, and find that it will always benefit the element to do so. Genes causing germline sequestration can therefore spread in a population even if germline sequestration is maladaptive for the host organism. Costly selfish elements are expected to survive only in sexual populations, so sexual species may experience an additional push toward germline-soma distinction, and hence toward cell differentiation and multicellularity.