Acorn barnacles are important model organisms for the study of sex allocation. They are sessile, nonselfing hermaphrodites that copulate with penises that have been suggested to be phenotypically plastic. On wave-exposed shores, Semibalanus balanoides develop penises with relatively greater diameter whereas in wave-protected sites they are thinner. A reciprocal transplant experiment between wave-exposed and protected sites tested whether these exposure-specific morphologies have adaptive value. Mating success was compared over a range of distances to compare the ability of barnacles to reach mates. Barnacles that grew in the wave-protected site and mated in the wave-protected site fertilized more broods at increasing distances than those transplanted to the wave-exposed site. For barnacles that developed in the wave-exposed site, there was no difference in the ability to fertilize neighbors between sites of differing exposure. This study demonstrates the adaptive value of plasticity in penis morphology. The results suggest a trade-off between development of a penis adapted to wave exposure and the ability to fertilize distant mates. Barnacles in different physical environments are limited by different factors, which may limit numbers of potential mates, constrain optimal sex allocation strategies and alter reproductive behavior.

The phenotypic plasticity of traits, defined as the ability of a genotype to express different phenotypic values of the trait across a range of environments, can vary between habitats depending on levels of temporal and spatial heterogeneity. Other traits can be insensitive to environmental perturbations and show environmental canalization. We tested levels of phenotypic plasticity in diverse Drosophila serrata populations along a latitudinal cline ranging from a temperate, variable climate to a tropical, stable climate by measuring developmental rate and size-related traits at three temperatures (16°C, 22°C, and 28°C). We then compared the slopes of the thermal reaction norms among populations. The 16–22°C part of the reaction norms for developmental rate was flatter (more canalized) for the temperate populations than for the tropical populations. However, slopes for the reaction norms of the two morphological traits (wing size, wing:thorax ratio), were steeper (more plastic) in the temperate versus the tropical populations over the entire thermal range. The different latitudinal patterns in plasticity for developmental rate and the morphological traits may reflect contrasting selection pressures along the tropical-temperate thermal gradient.

Extinctions of local subpopulations are common events in nature. Here, we ask whether such extinctions can affect the design of biological networks within organisms over evolutionary timescales. We study the impact of extinction events on modularity of biological systems, a common architectural principle found on multiple scales in biology. As a model system, we use networks that evolve toward goals specified as desired input-output relationships. We use an extinction—recolonization model, in which metapopulations occupy and migrate between different localities. Each locality displays a different environmental condition (goal), but shares the same set of subgoals with other localities. We find that in the absence of extinction events, the evolved computational networks are typically highly optimal for their localities with a nonmodular structure. In contrast, when local populations go extinct from time to time, we find that the evolved networks are modular in structure. Modular circuitry is selected because of its ability to adapt rapidly to the conditions of the free niche following an extinction event. This rapid adaptation is mainly achieved through genetic recombination of modules between immigrants from neighboring local populations. This study suggests, therefore, that extinctions in heterogeneous environments promote the evolution of modular biological network structure, allowing local populations to effectively recombine their modules to recolonize niches.

Many trophically transmitted parasites have complex life cycles: they pass through at least one intermediate host before reproducing in their final host. Despite their economic and theoretical importance, the evolution of such cycles has rarely been investigated. Here, combining a novel modeling approach with experimental data, we show for the first time that an optimal transfer time between hosts exists for a “model parasite,” the tapeworm Schistocephalus solidus, from its first (copepod) to its second (fish) intermediate host. When transferring between hosts around this time, (1) parasite performance in the second intermediate host, (2) reproductive success in the final host, and (3) fitness in the next generation is maximized. At that time, the infected copepod's behavior changes from predation suppression to predation enhancement. The optimal time for switching manipulation results from a trade-off between increasing establishment probability in the next host and reducing mortality in the present host. Our results show that these manipulated behavioral changes are adaptive for S. solidus, rather than an artifact, as they maximize parasite fitness.

In moth pheromone communication signals, both quantitative and qualitative intraspecific differences have been found across geographic regions. Such variation has generally been hypothesized to be due to selection, but evidence of genetic control of these differences is largely lacking. To explore the patterns of variation in pheromone signals, we quantified variation in the female sex pheromone blend and male responses of two closely related noctuid moth species in five different geographic regions for 2–3 consecutive years. We found significant variation in the ratios of sex pheromone blend components as well as in male response, not only between geographic regions but also within a region between consecutive years. The temporal variation was of a similar magnitude as the geographic variation. As far as we know, this is the first study reporting such temporal variation in moth chemical communication systems. The geographic variation seems to at least partly be controlled by genetic factors, and to be correlated with the quality of the local chemical environment. However, the pattern of temporal variation within populations suggests that optimization of the pheromonal signal also may be driven by within-generation physiological adjustments by the moths in response to their experience of the local chemical environment.

Adaptive divergence between adjoining populations reflects a balance between the diversifying effect of divergent selection and the potentially homogenizing effect of gene flow. In most models of migration-selection balance, gene flow is assumed to reflect individuals' inherent capacity to disperse, without regard to the match between individuals' phenotypes and the available habitats. However, habitat preferences can reduce dispersal between contrasting habitats, thereby alleviating migration load and facilitating adaptive divergence. We tested whether habitat preferences contribute to adaptive divergence in a classic example of migration-selection balance: parapatric lake and stream populations of three-spine stickleback (Gasterosteus aculeatus). Using a mark-transplant-recapture experiment on morphologically divergent parapatric populations, we showed that 90% of lake and stream stickleback returned to their native habitat, reducing migration between habitats by 76%. Furthermore, we found that dispersal into a nonnative habitat was phenotype dependent. Stream fish moving into the lake were morphologically more lake-like than those returning to the stream (and the converse for lake fish entering the stream). The strong native habitat preference documented here increases the extent of adaptive divergence between populations two- to fivefold relative to expectations with random movement. These results illustrate the potential importance of adaptive habitat choice in driving parapatric divergence.

Extreme morphologies of many insular taxa suggest that islands have unusual properties that influence the tempo and mode of evolution. Yet whether insularity per se promotes rapid phenotypic evolution remains largely untested. We extend a phylogenetic comparative approach to test the influence of novel environments versus insularity on rates of body size and sexual size dimorphism diversification in Anolis. Rates of body size diversification among small-island and mainland species were similar to those of anole species on the Greater Antilles. However, the Greater Antilles taxa that colonized small islands and the mainland are ecologically nonrandom: rates of body size diversification among small-island and mainland species are high compared to their large-island sister taxa. Furthermore, rates of diversification in sexual size dimorphism on small islands are high compared to all large-island and mainland lineages. We suggest that elevated diversifying selection, particularly as a result of ecological release, may drive high rates of body size diversification in both small-island and mainland novel environments. In contrast, high abundance (prevalent among small-island lizard communities) mediating intraspecific resource competition and male—male competition may explain why sexual size dimorphism diversifies faster among small-island lineages than among their mainland and large-island relatives.

Population-specific preferences involved in premating isolation may be based on several different types of mating cues. Here, we compare the rates of spread of 12 different mating preferences that reflect preferences for local adaptation, male condition, and reinforcement. We introduce methods to dissect the components of the rate of spread to determine why certain mating preferences spread more quickly than others. We confirm the result that female preferences based on population-specific markers alone always spread faster than female preferences based only on a single local adaptation locus, regardless of the strength of natural selection on hybrid incompatibility. However, we find that this occurs for different reasons depending on the strength of selection against hybrids. Female preferences based on total male condition also achieved high rates of spread, suggesting that preferences for condition-dependent male displays may evolve under reinforcement scenarios.

The effect of inbreeding and outbreeding depression on the evolution of assortment are often considered separately. For instance, inbreeding depression is usually thought to shape selfing rates whereas outbreeding depression is commonly thought to affect the evolution of assortative mating. In this article, we consider the evolution of assortment in a context of local adaptation and we show that it is a typical situation in which both effects act simultaneously to shape the degree of selfing or assortative mating. More specifically, we show that selection on a modifier of mating can be partitioned into three distinct effects: a transmission advantage, an association to heterozygosity (proportional to inbreeding depression), and an association to beneficial alleles (proportional to outbreeding depression), so that random mating may evolve even with strong local adaptation. In addition, we show that it is necessary to carefully delimit the conditions for polymorphism at local adaptation locus to study the evolution of assortment. In particular, the range of parameters most favorable to the maintenance of polymorphism corresponds to situations favoring less assortment.

While speciation can be found in the presence of gene flow, it is not clear what impact this gene flow has on genome- and range-wide patterns of differentiation. Here we examine gene flow across the entire range of the common sunflower, H. annuus, its historically allopatric sister species H. argophyllus and a more distantly related, sympatric relative H. petiolaris. Analysis of genotypes at 26 microsatellite loci in 1015 individuals from across the range of the three species showed substantial introgression between geographically proximal populations of H. annuus and H. petiolaris, limited introgression between H. annuus and H. argophyllus, and essentially no gene flow between the allopatric pair, H. argophyllus and H. petiolaris. Analysis of sequence divergence levels among the three species in 1420 orthologs identified from EST databases identified a subset of loci showing extremely low divergence between H. annuus and H. petiolaris and extremely high divergence between the sister species H. annuus and H. argophyllus, consistent with introgression between H. annuus and H. petiolaris at these loci. Thus, at many loci, the allopatric sister species are more genetically divergent than the more distantly related sympatric species, which have exchanged genes across much of the genome while remaining morphologically and ecologically distinct.

The lichen-forming fungal genus Peltigera includes a number of species that are extremely widespread, both geographically and ecologically. However, morphological variability has lead to doubts about the distinctness of some species, and it has been suggested that hybridization is common in nature. We examined species boundaries by looking for evidence of hybridization and gene flow among seven described species collected at five sites in British Columbia, Canada. We found no evidence of gene flow or hybridization between described species, with fixed differences between species for two or more of the three loci examined. Reproductive isolation did not reflect a solely clonal mode of reproduction as there was evidence of ongoing gene flow within species. In addition, we found five undescribed species that were reproductively isolated, although there was evidence of ongoing or historical gene flow between two of the new species. These results indicate that the genus Peltigera is more diverse in western North America than originally perceived, and that morphological variability is due largely to the presence of undescribed species rather than hybridization or intraspecific variation.

Rapid evolution has been well documented in naturally selected traits, but few examples exist for sexually selected traits, particularly sexual signals. This may in part be due to the complex set of behaviors associated with sexual signals. For a sexual signal to change, the change must be favorable for the signaler, but must also be accommodated by the receiver's perception and preferences. We investigated female accommodation of an extreme change in the sexual signal of Polynesian field crickets, Teleogryllus oceanicus. The cricket is native to Australia, widely distributed on Pacific Islands, and was recently introduced to Hawaii. Selective pressure by a deadly parasitoid fly favored a wing mutation in Hawaii (flatwing) that eliminates males' singing ability altogether Despite conventional wisdom that females require males to produce a courtship song before mating, we show that females from ancestral, unparasitized Australian and Pacific Island populations as well as parasitized Hawaiian populations, will mate with silent flatwing males, suggesting this behavioral option predates the change in sexual signal. Furthermore, ancestral Australian females discriminate against flatwing males more severely than island females. We suggest island colonization favored females with relaxed mating requirements (Kaneshiro's effect) facilitating the rapid evolutionary loss of song in Hawaii.

Sporophytic self-incompatibility (SSI) is a self-pollen recognition system that enforces outcrossing in plants. Recognition in SSI systems is typically controlled by a complex locus (5-locus) with separate genes that determine pollen and stigma specificity. Experimental studies show that S-alleles can be dominant, recessive, or codominant, and that the dominance level of a given S-allele can depend upon whether pollen or stigma specificity is examined. Here and in the companion paper by Llaurens and colleagues, the evolution of dominance in single-locus SSI is explored using numerical models and simulation. Particular attention is directed at factors that can cause S-allele dominance to differ in pollen versus stigma. The effect of recombination between the S-locus and modifier locus is also examined. The models predict that limitation in the number of compatible mates is required for the evolution of S-allele dominance in the stigma but not in the pollen. Tight linkage between the S-locus and modifier promotes the evolution of S-allele dominance hierarchies. Model results are interpreted with respect to published information on the molecular basis of dominance in SSI systems, and reported S-allele dominance relationships in a variety of species. These studies show that dominant S-alleles are more common in the pollen than in the stigma, a pattern that when interpreted in light of model predictions, suggests that mate limitation may be relatively infrequent in natural populations with SSI.

Animal vocalizations play an important role in individual recognition, kin recognition, species recognition, and sexual selection. Despite much work in these fields done on birds virtually nothing is known about the heritability of vocal traits in birds. Here, we study a captive population of more than 800 zebra finches (Taeniopygia guttata) with regard to the quantitative genetics of call and song characteristics. We find very high heritabilities in nonlearned female call traits and considerably lower heritabilities in male call and song traits, which are learned from a tutor and hence show much greater environmental variance than innate vocalizations. In both sexes, we found significant heritabilities in several traits such as mean frequency and measures of timbre, which reflect morphological characteristics of the vocal tract. These traits also showed significant genetic correlations with body size, as well as positive genetic correlations between the sexes, supporting a scenario of honest signaling of body size through genetic pleiotropy (“index signal”). In contrast to such morphology-related voice characteristics, classical song features such as repertoire size or song length showed very low heritabilities. Hence, these traits that are often suspected to be sexually selected would hardly respond to current directional selection.

The Red Queen hypothesis argues that parasites generate selection for genetic mixing (sex and recombination) in their hosts. A number of recent papers have examined this hypothesis using models with haploid hosts. In these haploid models, sex and recombination are selectively equivalent. However, sex and recombination are not equivalent in diploids because selection on sex depends on the consequences of segregation as well as recombination. Here I compare how parasites select on modifiers of sexual reproduction and modifiers of recombination rate. Across a wide set of parameters, parasites tend to select against both sex and recombination, though recombination is favored more often than is sex. There is little correspondence between the conditions favoring sex and those favoring recombination, indicating that the direction of selection on sex is often determined by the effects of segregation, not recombination. Moreover, when sex was favored it is usually due to a long-term advantage whereas short-term effects are often responsible for selection favoring recombination. These results strongly indicate that Red Queen models focusing exclusively on the effects of recombination cannot be used to infer the type of selection on sex that is generated by parasites on diploid hosts.

In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.

We applied QTL mapping to fitness variation of Avena barbata under well-watered greenhouse conditions. One hundred eighty recombinant inbred lines were assayed for flowering time, total size, mass allocation, and fitness. Composite Interval Mapping identified two to five loci affecting these traits. These were well supported in more powerful Multiple and Bayesian interval mapping analyses that indicated that additional QTL, as well as epistatic interactions also affect the traits. The posterior distribution of the number of QTL peaked at five to eight additive loci and one to two interactions, but the specific locations of the additional loci could not be determined with certainty. In most cases in which loci for separate traits mapped to similar locations, explicit tests supported pleiotropy over close linkage of separate loci. Alleles that hastened first flowering generally reduced vegetative mass, increased reproductive mass, and were associated with high fitness. Because effects on mass allocation generally cancelled one another, few loci affected total plant size. Only one QTL affected vegetative mass independent of reproductive mass and this locus had little effect on fitness. Thus selection acts to shift the mass allocation toward greater reproductive allocation, because the correlated decrease in vegetative mass poses only a minor fitness cost.

Most experimentally detectable effects of mutations in cellular organisms are either lethal or mildly deleterious. A possible explanation for the paucity of strongly detrimental but nonlethal mutations is that the processes constituting cellular metabolism are either essential or largely redundant. Alternatively, the partition between lethal and inconspicuous mutations exists within important biological processes. To test this, we measured maximum growth rates of yeast strains each carrying the deletion of a single gene in one of 38 protein complexes. We also used relevant data from previous high-throughput phenotypic studies of the yeast gene-deletion collection. The complexes typified well-defined sets of genes engaged in a common process. Within virtually all essential complexes there were two clear modes of phenotypic effects, that is the cessation of growth or slowdown of growth by a few percent. This uniformity is striking given that complexes differ extensively in function, size, and proportion of essential proteins. The pattern of bimodality is observed both under optimal and suboptimal environmental conditions. The generic paucity of strong effects and abundance of small ones relates to the feasibility of analyses of quantitative traits and epidemiological surveys, irrespective of the particular element of metabolism under study.

The ∼50 million-year-old fungus-farming ant mutualism is a classic example of coevolution, involving ants that subsist on asexual, fungal biomass, in turn propagating the fungus clonally through nest-to-nest transmission. Most mutualistic ants cultivate two closely related groups of gilled mushrooms, whereas one small group of ants in the genus Apterostigma cultivates a distantly related lineage comprised of the G2 and G4 groups. The G2 and G4 fungi were previously shown to form a monophyletic group sister to the thread-like coral mushroom family Pterulaceae. Here, we identify an enigmatic coral mushroom that produces both fertile and sterile fruiting structures as the closest free-living relative of the G4 fungi, challenging the monophyly of the Apterostigma-cultivated fungi for the first time. Both nonparametric bootstrap and Bayesian posterior probability support the node leading to the G4 cultivars and a free-living Pterula mushroom. These data suggest three scenarios that contradict the hypothesis of strict coevolution: (1) multiple domestications, (2) escape from domestication, (3) selection of single cultivar lineages from an ancestral mixed-fungus garden. These results illustrate how incomplete phylogenies for coevolved symbionts impede our understanding of the patterns and processes of coevolution.

Genetic variation can be beneficial to one sex yet harmful when expressed in the other—a condition referred to as sexual antagonism. Because X chromosomes are transmitted from fathers to daughters, and sexually antagonistic fitness variation is predicted to often be X-linked, mates of relatively low-fitness males might produce high-fitness daughters whereas mates of high-fitness males produce low-fitness daughters. Such fitness consequences have been predicted to influence the evolution of female mating biases and the offspring sex ratio. Females might evolve to prefer mates that provide good genes for daughters or might adjust offspring sex ratios in favor of the sex with the highest relative fitness. We test these possibilities in a laboratory-adapted population of Drosophila melanogaster, and find that females preferentially mate with males carrying genes that are deleterious for daughters. Preferred males produce equal numbers of sons and daughters, whereas unpreferred males produce female-biased sex ratios. As a consequence, mean offspring fitness of unpreferred males is higher than offspring fitness of preferred males. This observation has several interesting implications for sexual selection and the maintenance of population genetic variation for fitness.

The prevalence of F2 hybrid breakdown in interpopulation crosses of the marine copepod Tigriopus californicus can be explained by disruption of coadapted gene complexes. This study further dissects the nature of hybrid gene interactions, revealing that parental populations may also harbor maladapted gene complexes. Diagnostic molecular markers (14) were assayed in reciprocal F2 hybrids to test for gene interactions affecting viability. Results showed some evidence of nuclear—nuclear coadaptation. Although there were no significant examples of pairwise linkage disequilibrium between physically unlinked loci, one of the two reciprocal crosses did show an overall excess of parental double homozygotes and an overall dearth of nonparental double homozygotes. In contrast, the nuclear—cytoplasmic data showed a stronger tendency toward maladaptation within the specific inbred lines used in this study. For three out of four loci with significant frequency differences between reciprocal F2, homozygotes were favored on the wrong cytoplasmic background. A separate study of reciprocal backcross hybrids between the same two populations (but different inbred lines) revealed faster development time when the full haploid nuclear genome did not match the cytoplasm. The occurrence of such suboptimal gene complexes may be attributable to effects of genetic drift in small, isolated populations.

In contrast to placentals, marsupials are born with forelimbs that are greatly developmentally advanced relative to their hind limbs. Despite significant interest, we still do not know why this is the case, or how this difference is achieved developmentally. Studies of prechondrogenic and chondrogenic limbs have supported the traditional hypothesis that marsupial forelimb development is accelerated in response to the functional requirements of the newborn's crawl to the teat. However, limb ossification studies have concluded that, rather than the forelimb being accelerated, hind limb development is delayed. By increasing the taxonomic coverage and number of prechondrogenic events relative to previous studies, and combining traditional phylogenetic analyses of event sequences with novel analyses of relative developmental rates, this study demonstrates that the timing of limb development in marsupials is more complex than commonly thought. The marsupial phenotype was derived through two independent evolutionary changes in developmental rate: (1) an acceleration of the forelimb's first appearance and (2) a delay of hind limb development from the bud stage onward. Surprisingly, this study also provides some support for an evolutionary acceleration of the marsupial hind limb's first appearance. Further study is needed on the developmental and genetic mechanisms driving these major evolutionary transitions.

Speciation can be driven by the evolution of many forms of reproductive isolation. Comparative study is a powerful approach for elucidating the relative importance of individual isolating barriers in the speciation process. A recent contribution by Scopece and colleagues provides comparative data for two groups of deceptive pollination orchids and aims to test hypotheses about which forms of isolation are most important in the two clades. The authors compare pollinator isolation and postmating isolation between the two orchid groups, and conclude that food-deceptive orchid species have less isolation by pollinator specificity than sexually deceptive species, and that postmating isolation is more important in the food-deceptive clade. Although we find this approach to be novel and potentially powerful, these conclusions are called into question by the methods used to define and select species and quantify pollinator isolation. Definition and selection of taxa were performed in a biased manner that undermines the ability to infer general patterns of speciation. Furthermore, pollinator isolation was calculated inconsistently for the two groups under study, effectively nullifying the comparison.

Sobel and Randle (2009) challenge several methodological choices in the comparative study of the evolution of reproductive isolation in Mediterranean deceptive orchids of Scopece et al. (2007) including the species concept used and the selection of taxa, together with the perceived comparison of clades of different ages. They further criticize that pollinator information was taken from the literature and that two different methods were used to estimate pollinator specificity in food-deceptive and sexually deceptive orchids, respectively. Here we reply to these challenges.