Extinction and the temporal distribution of macroevolutionary bursts.

Phenotypic evolution through deep time is slower than expected from microevolutionary rates. This is the paradox of stasis. Previous models suggest stasis occurs because populations track adaptive peaks that remain relatively stable on million-year intervals, raising the equally perplexing question of why these large changes are so rare. Here, we consider the possibility that peaks can move more rapidly than populations can adapt, resulting in extinction. We model peak movement with explicit population dynamics, parameterized with published microevolutionary estimates. Allowing extinction greatly increases the parameter space of peak movements that yield the appearance of stasis observed in real data through deep time. Extreme peak displacements, regardless of their frequency, will rarely result in an equivalent degree of trait evolution because of extinction. Thus, larger peak displacements will rarely be inferred using trait data from extant species or observed in fossil records. Our work highlights population ecology as an important contributor to macroevolutionary dynamics, presenting an alternative perspective on the paradox of stasis, where apparent constraint on phenotypic evolution in deep time reflects our restricted view of the subset of earth's lineages that were fortunate enough to reside on relatively stable peaks.

Climate change has different predicted effects on the range shifts of two hybridizing ambush bug (Phymata, Family Reduviidae, Order Hemiptera) species.

AIM: A universal attribute of species is that their distributions are limited by numerous factors that may be difficult to quantify. Furthermore, climate change-induced range shifts have been reported in many taxa, and understanding the implications of these shifts remains a priority and a challenge. Here, we use Maxent to predict current suitable habitat and to project future distributions of two closely related, parapatrically distributed Phymata species in light of anthropogenic climate change. LOCATION: North America. TAXON: Phymata americana Melin 1930 and Phymata pennsylvanica Handlirsch 1897, Family: Reduviidae, Order: Hemiptera. METHODS: We used the maximum entropy modeling software Maxent to identify environmental variables maintaining the distribution of two Phymata species, Phymata americana and Phymata pennsylvanica. Species occurrence data were collected from museum databases, and environmental data were collected from WorldClim. Once we gathered distribution maps for both species, we created binary suitability maps of current distributions. To predict future distributions in 2050 and 2070, the same environmental variables were used, this time under four different representative concentration pathways: RCP2.6, RCP4.5, RCP6.0, and RCP8.5; as well, binary suitability maps of future distributions were also created. To visualize potential future hybridization, the degree of overlap between the two Phymata species was calculated. RESULTS: The strongest predictor to P. americana ranges was the mean temperature of the warmest quarter, while precipitation of the driest month and mean temperature of the warmest quarter were strong predictors of P. pennsylvanica ranges. Future ranges for P. americana are predicted to increase northwestward at higher CO2 concentrations. Suitable ranges for P. pennsylvanica are predicted to decrease with slight fluctuations around range edges. There is an increase in overlapping ranges of the two species in all future predictions. MAIN CONCLUSIONS: These evidences for different environmental requirements for P. americana and P. pennsylvanica account for their distinct ranges. Because these species are ecologically similar and can hybridize, climate change has potentially important eco-evolutionary ramifications. Overall, our results are consistent with effects of climate change that are highly variable across species, geographic regions, and over time.

The strength of sex-specific selection in the wild.

Anisogamy predisposes the sexes to very different patterns of selection on shared traits. Selective differences between the sexes may manifest as changes in the direction or strength of selection acting on shared phenotypes. Although previous studies have found evidence for widespread differences in the direction of selection between the sexes, surprisingly little is known regarding potential differences in the magnitude of selection and whether such differences might be confined to specific components of fitness. We conducted a meta-analysis using 865 estimates of phenotypic selection from wild populations to characterize sex differences in the strength of selection and to ask whether different components of fitness exhibit differences in sex bias in the strength of selection. Overall, consistent with past results, we find evidence of male bias in the strength of selection, driven primarily by components of fitness related to mating success and we discuss several evolutionary implications.

Concordance between stabilizing sexual selection, intraspecific variation, and interspecific divergence in Phymata.

Empirical studies show that lineages typically exhibit long periods of evolutionary stasis and that relative levels of within-species trait covariance often correlate with the extent of between-species trait divergence. These observations have been interpreted by some as evidence of genetic constraints persisting for long periods of time. However, an alternative explanation is that both intra- and interspecific variation are shaped by the features of the adaptive landscape (e.g., stabilizing selection). Employing a genus of insects that are diverse with respect to a suite of secondary sex traits, we related data describing nonlinear phenotypic (sexual) selection to intraspecific trait covariances and macroevolutionary divergence. We found support for two key predictions (1) that intraspecific trait covariation would be aligned with stabilizing selection and (2) that there would be restricted macroevolutionary divergence in the direction of stabilizing selection. The observed alignment of all three matrices offers a point of caution in interpreting standing variability as metrics of evolutionary constraint. Our results also illustrate the power of sexual selection for determining variation observed at both short and long timescales and account for the apparently slow evolution of some secondary sex characters in this lineage.

Evolution of sexual dimorphism in phenotypic covariance structure in Phymata.

Sexual dimorphism is a consequence of both sex-specific selection and potential constraints imposed by a shared genetic architecture underlying sexually homologous traits. However, genetic architecture is expected to evolve to mitigate these constraints, allowing the sexes to approach their respective optimal mean phenotype. In addition, sex-specific selection is expected to generate sexual dimorphism of trait covariance structure (e.g., the phenotypic covariance matrix, P), but previous empirical work has not fully addressed this prediction. We compared patterns of phenotypic divergence, for three traits in seven taxa in the insect genus Phymata (Reduviidae), to ask whether sexual dimorphism in P is common and whether its magnitude relates to the extent of sexual dimorphism in trait means. We found that sexual dimorphism in both mean and covariance structure was pervasive but also that the multivariate distance between sex-specific means was correlated with sex differences in the leading eigenvector of P, while accounting for uncertainty in phylogenetic relationships. Collectively, our findings suggest that sexual dimorphism in covariance structure may be a common but underappreciated feature of dioecious populations.

Multivariate phenotypic divergence due to the fixation of beneficial mutations in experimentally evolved lineages of a filamentous fungus.

The potential for evolutionary change is limited by the availability of genetic variation. Mutations are the ultimate source of new alleles, yet there have been few experimental investigations of the role of novel mutations in multivariate phenotypic evolution. Here, we evaluated the degree of multivariate phenotypic divergence observed in a long-term evolution experiment whereby replicate lineages of the filamentous fungus Aspergillus nidulans were derived from a single genotype and allowed to fix novel (beneficial) mutations while maintained at two different population sizes. We asked three fundamental questions regarding phenotypic divergence following approximately 800 generations of adaptation: (1) whether divergence was limited by mutational supply, (2) whether divergence proceeded in relatively many (few) multivariate directions, and (3) to what degree phenotypic divergence scaled with changes in fitness (i.e. adaptation). We found no evidence that mutational supply limited phenotypic divergence. Divergence also occurred in all possible phenotypic directions, implying that pleiotropy was either weak or sufficiently variable among new mutations so as not to constrain the direction of multivariate evolution. The degree of total phenotypic divergence from the common ancestor was positively correlated with the extent of adaptation. These results are discussed in the context of the evolution of complex phenotypes through the input of adaptive mutations.

Correlation of mycelial growth rate with other phenotypic characters in evolved genotypes of Aspergillus nidulans.

Fungal populations can adapt to their environment by the generation and fixation of spontaneous beneficial mutations. In this study we examined whether adaptation, measured as an increased mycelial growth rate, has correlated responses in the filamentous fungus Aspergillus nidulans with several other metric characters that could be important fitness components (colony forming units, germination speed, and biomass formation). Studying 60 populations that had evolved over 800 generations by experimental evolution, we find that only mycelial growth rate increased during adaptation to growing on solid medium. We further found that among evolved strains colony forming units is negatively correlated with mycelial growth rate and that colony forming units and biomass formation show a positive correlation. Our results give insight into changes in fungal phenotype as a result of adaptation and suggest that mycelial growth rate is the only available target of selection.

Sexual dimorphism: why the sexes are (and are not) different.

Sex differences often call sexual selection to mind; however, a new damselfly study cautions on being too hasty, and implicates viability selection in the evolution of male and female colouration.

Temporally variable multivariate sexual selection on sexually dimorphic traits in a wild insect population.

A widely held view is that the strength and form of natural selection varies in time and space in response to varying ecological forces; however, adequate quantitative evaluations of this are relatively scarce. In this study, we measured the strength and form of sexual selection acting on a suite of male morphological traits in a wild ambush bug (Phymata americana) population at 10 sampling dates over 2 years. We tested the prediction that the strength and direction of sexual selection would be associated with one or more important ecological variables. We found that patterns of multivariate selection varied considerably over time, and even within a season. Yet, for this population, a sexually dimorphic color pattern trait was consistently a target of directional selection. The strength of sexual selection on this trait was related to both sex ratio and density, which is consistent with the idea that ecological factors can play an important role in generating patterns of sexual selection. We also demonstrate that the median strength of linear selection obtained from replicated cross-sectional methods was qualitatively similar to the estimates obtained from longitudinal methods, providing multiple lines of evidence that the evolution of sexual color dimorphism in this species is attributable to sexual selection.

Do female fruit flies (Drosophila serrata) copy the mate choice of others?

Female mate-choice copying is a social learning phenomenon whereby a female's observation of a successful sexual interaction between a male and another female increases her likelihood of subsequently preferring that male. Although mate-choice copying has been documented in several vertebrate species, to our knowledge it has not yet been investigated in insects. Here, we investigated whether female mate-choice copying occurs in the fruit fly Drosophila serrata, a model system for the study of mate preferences and the sexual selection they generate. We used two complementary experiments in which focal females were given a choice between two males that differed in either their apparent (as determined visually by the focal female) or actual recent mating success. Mate-choice copying was evaluated by testing whether focal females mated more frequently with the 'preferred' male as opposed to the other male. In both experiments, however, we found no evidence for mate-choice copying. We discuss possible reasons for the apparent absence of mate-choice copying in this species.

Experience affects the outcome of agonistic contests without affecting the selective advantage of size.

In the field, phenotypic determinants of competitive success are not always absolute. For example, contest experience may alter future competitive performance. As future contests are not determined solely on phenotypic attributes, prior experience could also potentially alter phenotype-fitness associations. In this study, we examined the influence of single and multiple experiences on contest outcomes in the jumping spider Phidippus clarus. We also examined whether phenotype-fitness associations altered as individuals gained more experience. Using both size-matched contests and a tournament design, we found that both winning and losing experience affected future contest success; males with prior winning experience were more likely to win subsequent contests. Although experience was a significant determinant of success in future contests, male weight was approximately 1.3 times more important than experience in predicting contest outcomes. Despite the importance of experience in determining contest outcomes, patterns of selection did not change between rounds. Overall, our results show that experience can be an important determinant in contest outcomes, even in short-lived invertebrates, and that experience alone is unlikely to alter phenotype-fitness associations.

Sexual selection mediated by the thermoregulatory effects of male colour pattern in the ambush bug Phymata americana.

Sexual dimorphism in coloration is a taxonomically widespread phenomenon often attributed to sexual selection on visual signals. However, the ambush bug Phymata americana exhibits sexual dimorphism in coloration that has no apparent signalling function. Here we provide evidence that colour pattern in this species influences male mating success indirectly through its effect on thermoregulation. We demonstrate, using experimental manipulation, that individuals with dark colour pattern achieve higher thoracic temperatures under illumination. We also show that dark colour pattern predicted mate-searching success but only under thermally challenging conditions (i.e. cool ambient temperature). As far as we are aware, this is the first study to provide evidence that sexual dimorphism can be accounted for by sexual selection on thermoregulatory performance.

Assessment during aggressive contests between male jumping spiders.

Assessment strategies are an important component in game theoretical models of contests. Strategies can be either based on one's own abilities (self assessment) or on the relative abilities of two opponents (mutual assessment). Using statistical methodology that allows discrimination between assessment types, we examined contests in the jumping spider Phiddipus clarus. In this species, aggressive interactions can be divided into 'pre-contact' and 'contact' phases. Pre-contact phases consist of bouts of visual and vibratory signaling. Contact phases follow where males physically contact each other (leg fencing). Both weight and vibratory signaling differences predicted winners with heavier and more actively signaling males winning more contests. Vibratory behaviour predicted pre-contact phase duration, with higher signaling rates and larger differences between contestants leading to longer pre-contact interaction times. Contact phase duration was predicted most strongly by the weight of losing males relative to that of winning males, suggesting that P. clarus males use self-assessment in determining contest duration. While a self-assessment strategy was supported, our data suggest a secondary role for mutual assessment ("partial mutual assessment"). After initial contest bouts, male competitors changed their behaviour. Pre-contact and contact phase durations were reduced while vibratory signaling behaviour in winners was unchanged. In addition, only vibratory signaling differences predicted winners in subsequent bouts suggesting a role of experience in determining contest outcomes. We suggest that the rules and assessment strategies males use can change depending on experience and that assessment strategies are likely a continuum between self- and mutual assessment.

Frequency-dependent survival in natural guppy populations.

The maintenance of genetic variation in traits under natural selection is a long-standing paradox in evolutionary biology. Of the processes capable of maintaining variation, negative frequency-dependent selection (where rare types are favoured by selection) is the most powerful, at least in theory; however, few experimental studies have confirmed that this process operates in nature. One of the most extreme, unexplained genetic polymorphisms is seen in the colour patterns of male guppies (Poecilia reticulata). Here we manipulated the frequencies of males with different colour patterns in three natural populations to estimate survival rates, and found that rare phenotypes had a highly significant survival advantage compared to common phenotypes. Evidence from humans and other species implicates frequency-dependent survival in the maintenance of molecular, morphological and health-related polymorphisms. As a controlled manipulation in nature, this study provides unequivocal support for frequency-dependent survival--an evolutionary process capable of maintaining extreme polymorphism.