Sensory trade-offs predict signal divergence in Surfperch

Unidirectional elaboration of male trait evolution (e.g., larger, brighter males) has been predicted by receiver bias models of sexual selection and empirically tested in a number of different taxa. This study identifies a bidirectional pattern of male trait evolution and suggests that a sensory constraint is driving this divergence. In this system, the inherent trade-off in dichromatic visual detection places limits on the direction that sensory biases may take and thus provides a quantitative test of the sensory drive model. Here I show that sensory systems with trade-offs in detection abilities produce bidirectional biases and that signal design properties match these biases. I combine species-specific measurements and ancestral estimates with visual detection modeling to examine biases in sensory and signaling traits across five fish species occupying optically diverse habitats in the Californian kelp forest. Species-specific divergence in visual pigments correlates with changes in environment and produces different sensory biases--favoring luminance (brightness) detection for some species and chromatic (color) detection for others. Divergence in male signals (spectral reflectance of orange, blue, and silver color elements) is predicted by each species' sensory bias: color divergence favors chromatic detection for species with chromatically biased visual systems, whereas species with luminance sensory biases have signals favoring luminance detection. This quantitative example of coevolution of communication traits varying in a bidirectional pattern governed by the environment is the first demonstration of sensory trade-offs driving signal evolution.     

The evolution of feeding motor patterns in vertebrates

Despite considerable skepticism, researchers have found that the patterns of muscle activation that control feeding behaviors of lower vertebrates have been surprisingly conserved during evolution. This tendency for conservation among taxa appears in the face of marked flexibility of motor patterns within individuals. One interpretation of these apparently conflicting trends is that the most effective motor pattern for any given feeding situation is the same across substantial phylogenetic distances and morphological differences. The novel evolutionary insight provided by this research is that historical changes to motor patterns are a relatively infrequent source of trophic innovation. The spectacular diversity of feeding abilities and feeding ecology in lower vertebrates is based mostly on axes of variation, and on the innovations in the organization of muscles and the skeletal linkage systems that they drive.     

Molecular evolution of the phytochrome gene family in sorghum: changing rates of synonymous and replacement evolution

The photoreceptor phytochromes, encoded by a small gene family, are responsible for controlling the expression of a number of light-responsive genes and photomorphogenic events, including agronomically important phenotypes such as flowering time and shade-avoidance behavior. The understanding and control of flowering time are particularly important goals in sorghum cultivar development for diverse environments, and naturally occurring variation in the phytochrome genes might prove useful in breeding programs. Also of interest is whether variation observed at the phytochrome loci in domesticated sorghum, or in particular races, is a result of human selection. Population genetic studies can reveal evidence of such selection in patterns of polymorphism and divergence. In this study we report a population genetic analysis of the PHY gene family in Sorghum bicolor (L.) Moench in a diverse panel including both cultivated and wild accessions. We show that the level of nucleotide variation in all gene family members is about half the average for this species, consistent with purifying selection acting on these loci. However, the rate of amino acid substitution is accelerated at PHYC compared to the other two loci. In comparisons to a closely related sorghum species, PHYC shows a pattern of intermediate frequency amino acid changes that differ from the patterns observed in comparisons across longer evolutionary distances. There is also a departure from expected patterns of polymorphism and divergence at synonymous sites in PHYC, although the data do not fit a simple model of directional or diversifying selection. Cultivated sorghum has a level of variation similar to that of wild relatives (ssp. verticilliflorum), but many polymorphisms are subspecies-specific, including several amino acid variants.     

The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex

The effective use of microsatellite loci as tools for microevolutionary analysis requires knowledge of the factors influencing the rate and pattern of mutation, much of which is derived from indirect inference from population samples. Interspecific variation in microsatellite stability also provides a glimpse into aspects of phylogenetic constancy of mutational processes. Using long-term series of mutation-accumulation lines, we have obtained direct estimates of the spectrum of microsatellite mutations in two model systems: the nematode Caenorhabditis elegans and the microcrustacean Daphnia pulex. Although the scaling of the mutation rate with the number of tandem repeats is highly consistent across distantly related species, including yeast and human, the per-cell-division mutation rate appears to be elevated in multicellular species. Contrary to the expectations under the stepwise mutation model, most microsatellite mutations in C. elegans and D. pulex involve changes of multiple repeat units, with expansions being much more common than contractions.     

EVOLUTION OF ALLORECOGNITION IN BOTRYLLID ASCIDIANS INFERRED FROM A MOLECULAR PHYLOGENY

Despite the functional and phyletic ubiquity of highly polymorphic genetic recognition systems, the evolution and maintenance of these remarkable loci remain an empirical and theoretical puzzle. Many clonal invertebrates use polymorphic genetic recognition systems to discriminate kin from unrelated individuals during behavioral interactions that mediate competition for space. Space competition may have been a selective force promoting the evolution of highly polymorphic recognition systems, or preexisting polymorphic loci may have been coopted for the purpose of mediating space competition. Ascidian species in the family Botryllidae have an allorecognition system in which fusion or rejection between neighboring colonies is controlled by allele-sharing at a single, highly polymorphic locus. The behavioral sequence involved in allorecognition varies in a species-specific fashion with some species requiring extensive intercolony tissue integration prior to the allorecognition response, while other species contact opposing colonies at only a few points on the outer surface before resolving space conflicts. Due to an apparent species-specific continuum of behavioral variation in the degree of intercolony tissue integration required for allorecognition, this system lends itself to a phylogenetic analysis of the evolution of an allorecognition system. We constructed a molecular phylogeny of the botryllids based on 18S rDNA sequence and mapped allorecognition behavioral variation onto the phylogeny. Our phylogeny shows the basal allorecognition condition for the group is the most internal form of the recognition reaction. More derived species show progressively more external allorecognition responses, and in some cases loss of some features of internal function. We suggest that external allorecognition appears to be a secondary function of a polymorphic discriminatory system that was already in place due to other selective pressures such as gamete, pathogen, or developmental cell lineage recognition.     

Directional evolution of size coupled with ascertainment bias for variation in Drosophila microsatellites

Species-specific differences in microsatellite locus length and ascertainment bias have both been proposed to explain differences in microsatellite variability and length usually observed when loci isolated in one species are used to survey variation in a related species. Here we provide a simple algebraic approach to independently estimate the contributions of true species-specific length differences and ascertainment bias. We apply this approach to a reciprocal-isolation microsatellite study and show contributions of both ascertainment bias and a true longer average microsatellite length in Drosophila melanogaster compared with D. simulans.     

Sensory-motor interactions modulate a primate vocal behavior: antiphonal calling in common marmosets

A fundamental issue in neuroscience pertains to how different cortical systems interact to generate behavior. One of the most direct ways to address this issue is to investigate how sensory information is encoded and used to produce a motor response. Antiphonal calling is a natural vocal behavior that involves individuals producing their species-specific long distance vocalization in response to hearing the same call and engages both the auditory and motor systems, as well as the cognitive neural systems involved in decision making and categorization. Here we present results from a series of behavioral experiments investigating the auditory–vocal interactions during antiphonal calling in the common marmoset (Callithrix jacchus). We manipulated sensory input by placing subjects in different social contexts and found that the auditory input had a significant effect on call timing and propensity to call. Playback experiments tested the significance of the timing of vocal production in antiphonal calling and showed that a short latency between antiphonal calls was necessary to maintain reciprocal vocal interactions. Overall, this study shows that sensory-motor interactions can be experimentally induced and manipulated in a natural primate vocal behavior. Antiphonal calling represents a promising model system to examine these issues in non-human primates at both the behavioral and neural levels.     

Rapid evolution of courtship song pattern in Drosophila willistoni sibling species

Courtship behaviours may provide a more reliable means of identifying reproductively isolated taxa than traits such as morphology or many genetic markers. Here we describe the courtship songs of the Drosophila willistoni sibling species group, which consists of several species and subspecies. We find that song pattern is species-specific, despite significant differences among strains within species. D. paulistorum has the most variable song pattern, which reflects this species' traditional subdivision into semispecies. All the other species could be unambiguously identified by song. The major differences among these species was in the interpulse interval, as has been found in other studies of fly song. However, the interpulse intervals of the species studied here were often multimodal. This was partly due to the presence of multiple song types within the courtship repertoire, but it also reflected changes in interpulse interval within a song type by some males. Unusually, some species had distinctively patterned variation in interpulse interval. Song must have evolved rapidly within the species complex, probably due to sexual selection.     

Antagonistic evolution in an aposematic predator–prey signaling system

Warning signals within species, such as the bright colors of chemically defended animals, are usually considered mutualistic, monomorphic traits. Such a view is however increasingly at odds with the growing empirical literature, showing nontrivial levels of signal variation within prey populations. Key to understanding this variation, we argue, could be a recognition that toxicity levels frequently vary within populations because of environmental heterogeneity. Inequalities in defense may undermine mutualistic monomorphic signaling, causing evolutionary antagonism between loci that determine appearance of less well‐defended and better defended prey forms within species. In this article, we apply a stochastic model of evolved phenotypic plasticity to the evolution of prey signals. We show that when toxicity levels vary, then antagonistic interactions can lead to evolutionary conflict between alleles at different signaling loci, causing signal evolution, “red queen‐like” evolutionary chase, and one or more forms of signaling equilibria. A key prediction is that variation in the way that predators use information about toxicity levels in their attack behaviors profoundly affects the evolutionary characteristics of the prey signaling systems. Environmental variation is known to cause variation in many qualities that organisms signal; our approach may therefore have application to other signaling systems.     

The evolution of neuronal circuits underlying species-specific behavior.

The nervous system is evolutionarily conservative compared to the peripheral appendages that it controls. However, species-specific behaviors may have arisen from very small changes in neuronal circuits. In particular, changes in neuromodulatory systems may allow multifunctional circuits to produce different sets of behaviors in closely related species. Recently, it was demonstrated that even species differences in complex social behavior may be attributed to a change in the promoter region of a single gene regulating a neuromodulatory action.     

Coalescent under the evolution of coadaptation

Adaptation to novel environments arises either from new beneficial mutations or by utilizing pre‐existing genetic variation. When standing variation is used as the source of new adaptation, fitness effects of alleles may be altered through an environmental change. Alternatively, changes in epistatic genetic backgrounds may convert formerly neutral mutations into beneficial alleles in the new genetic background. By extending the coalescent theory to describe the genealogical histories of two interacting loci, I here investigated the hitchhiking effect of epistatic selection on the amount and pattern of sequence diversity at the linked neutral regions. Assuming a specific form of epistasis between two new mutations that are independently neutral, but together form a coadapted haplotype, I demonstrate that the footprints of epistatic selection differ markedly between the interacting loci depending on the order and relative timing of the two mutational events, even though both mutations are equally essential for the formation of an adaptive gene combination. Our results imply that even when neutrality tests could detect just a single instance of adaptive substitution, there may, in fact, be numerous other hidden mutations that are left undetected, but still play indispensable roles in the evolution of a new adaptation. We expect that the integration of the coalescent framework into the general theory of polygenic inheritance would clarify the connection between factors driving phenotypic evolution and their consequences on underlying DNA sequence changes, which should further illuminate the evolutionary foundation of coadapted systems.     

Ecology and signal structure drive the evolution of synchronous displays*

Animal synchrony is found in phylogenetically distant animal groups, indicating behavioral adaptations to different selective pressures and in different signaling modalities. A notable example of synchronous display is found in fiddler crabs in that males wave their single enlarged claw during courtship. They present species-specific signals, which are composed of distinctive movement signatures. Given that synchronous waving has been reported for several fiddler crab species, the display pattern could influence the ability of a given species to sufficiently adjust wave timing to allow for synchrony. In this study, we quantified the wave displays of fiddler crabs to predict their synchronous behavior. We combined this information with the group's phylogenetic relationships to trace the evolution of display synchrony in an animal taxon. We found no phylogenetic signal in interspecific variation in predicted wave synchrony, which mirrors the general nonphylogenetic pattern of synchrony across animal taxa. Interestingly, our analyses show that the phenomenon of synchronization stems from the peculiarities of display pattern, mating systems, and the complexity of microhabitats. This is the first study to combine mathematical simulations and phylogenetic comparative methods to reveal how ecological factors and the mechanics of animal signals affect the evolution of the synchronous phenomena.     

Leaf trait variation captures climate differences but differs with species irrespective of functional group

Aims To clarify whether variation in leaf traits with climate differs with scale, i.e. across species and within a species, and to detect whether plant functional group affects species-specific response.Methods Leaf dry matter content (LDMC), specific leaf area (SLA), mass- and area-based leaf N (N mass, N area) and leaf P concentrations (P mass, P area) and leaf chlorophyll concentration (SPAD) were measured for 92 woody plant species in two botanical gardens in China. The two gardens share plant species in common but differ in climate. Leaf trait variation between the two gardens was examined via mean comparison at three scales: all species together, species grouped into plant functional groups and within a species. A meta-analysis was performed to summarize the species-specific responses.Important findings At the scale of all species together, LDMC, SLA, P mass and N mass were significantly lower in the dry-cold habitat than in the wet-warm one, whereas N area and SPAD showed an inverse pattern, indicating a significant environmental effect. The meta-analysis showed that the above-mentioned patterns persisted for SLA, N area and SPAD but not for the other variables at the species-specific scale, indicating that intraspecific variation affects the overall pattern of LDMC, P mass and N mass and P area. In terms of species-specific response, positive, negative or nonsignificant patterns were observed among the 92 species. Contrary to our prediction, species-specific responses within a functional group were not statistically more similar than those among functional groups. Our results indicated that leaf trait variation captured climatic difference yet species-specific responses were quite diverse irrespective of plant functional group, providing new insights for interpreting trait variability with climate.     

Negative covariance suggests mutation bias in a two-locus microsatellite system in the fish Sparus aurata.

Constraints on microsatellite length appear to vary in a species-specific manner. We know very little about the nature of these constraints and why they should vary among species. While surveying microsatellite variation in the Mediterranean gilthead sea bream, Sparus aurata, we discovered an unusual pattern of covariation between two closely linked microsatellite loci. One- and two-locus haplotypes were scored from PCR amplification products of each locus separately and both loci together. In a sample of 211 fish, there was a strong negative covariance in repeat number between the two loci, which suggests a mechanism that maintains the combined length below a constrained size. In addition, there were two clusters of the same combined haplotype length, one consisting of a long repeat array at one locus and a short array at the other and vice versa. We demonstrate that several models of biased mutation or natural selection, in theory, could generate this pattern of covariance. The common feature of all the models is the idea that tightly linked microsatellites do not evolve in complete independence, and that whatever size dependence there is to the process, it appears to "read" the combined size of the two loci.     

How insects sense olfactory patches – the spatial scaling of olfactory information

When searching for resources in heterogeneous environments, animals must rely on their abilities to detect the resources via their sensory systems. However, variation in the strength of the sensory cue may be mediated by the physical size of the resource patch. Patch detection of insects are often predicted by the scaling of sensory cues to patch size, where visual cues has been proposed to scale proportional to the diameter of the patch. The scaling properties of olfactory cues are, however, virtually unknown. Here, we investigated scaling rules for olfactory information in a gradient of numbers of odour sources, relevant to odour‐mediated attraction under field conditions. We recorded moth antennal responses to sex pheromones downwind from pheromone patches and estimated the slope in the scaling relationship between the effective length of the odour plumes and the number of odour sources. These measurements showed that the effective plume length increased proportional to the square root of the number of odour sources. The scaling relationship, as estimated in the field experiment, was then evaluated against field data of the slope in the relationship between trap catch and release rate of chemical attractants for a wide range of insects. This meta‐analysis revealed an average slope largely consistent with the estimated scaling relationship between the effective plume length and the number of odour sources. This study is the first to estimate the scaling properties of olfactory cues empirically and has implications for understanding and predicting the spatial distributions of insects searching by means of olfactory cues in heterogeneous environments.     

Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin

Bindin is a gamete recognition protein of sea urchins that mediates species-specific attachment of sperm to an egg-surface receptor during fertilization. Sequences of bindin from closely related urchins show fixed species-specific differences. Within species, highly polymorphic bindin alleles result from point substitution, insertion/deletion, and recombination. Since speciation, positive selection favoring allelic variants has generated diversity in bindin polypeptides. Intraspecific bindin variation can be tolerated by the egg receptor, which suggests functional parallels between this system and other flexible recognition systems, including immune recognition. These results show that polymorphism in mate recognition loci required for rapid evolution of sexual isolation can arise within natural populations.      

Clines and adaptive evolution in the methuselah gene region in Drosophila melanogaster

In an effort to characterize further the patterns of selection and adaptive evolution at the methuselah locus in Drosophila species, we extended an analysis of geographical variation to include single nucleotide polymorphisms (SNPs) in adjacent genes on either side of the mth locus, and examined the molecular variation in a neighbouring methuselah paralogue (mth2). An analysis of 13 SNPs spanning a region of nearly 19 kilobases surrounding the mth locus demonstrated that a clinal pattern associated with the most common mth haplotype does not extend to adjacent gene loci, providing compelling evidence that the clinal pattern results from selection on as yet unidentified sites associated with the functional mth locus. mth2 exhibited a significant pattern of adaptive divergence among D. melanogaster, D. simulans and D. yakuba similar to that seen at mth. However, Ka : Ks ratios indicate a difference in levels of functional constraint at the two methuselah, loci with mth2 exhibiting a five- to six-fold reduction in levels of amino acid divergence relative to mth.     

The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores

Although recent evidence indicates that coevolutionary interactions between species often vary on a biogeographical scale, little consideration has been given to the processes responsible for producing this pattern. One potential explanation is that changes in the community composition alter the coevolutionary interactions between species, but little evidence exists regarding the occurrence of such changes. Here we present evidence that the pattern of natural selection on plant defence traits, and the probable response to that selection, are critically dependent on the composition of the biotic community. The evolutionary trajectory of defence traits against mammalian herbivory in the Ivyleaf morning glory (Ipomoea hederacea), and which defence traits are likely to respond to selection, are both dependent on the presence or absence of insect herbivores. These results indicate that variation in community composition may be a driving force in generating geographical mosaics.     

Signatures of selection and sex-specific expression variation of a novel duplicate during the evolution of the Drosophila desaturase gene family

The tempo and mode of evolution of loci with a large effect on adaptation and reproductive isolation will influence the rate of evolutionary divergence and speciation. Desaturase loci are involved in key biochemical changes in long-chain fatty acids. In insects, these have been shown to influence adaptation to starvation or desiccation resistance and in some cases act as important pheromones. The desaturase gene family of Drosophila is known to have evolved by gene duplication and diversification, and at least one locus shows rapid evolution of sex-specific expression variation. Here, we examine the evolution of the gene family in species representing the Drosophila phylogeny. We find that the family includes more loci than have been previously described. Most are represented as single-copy loci, but we also find additional examples of duplications in loci which influence pheromone blends. Most loci show patterns of variation associated with purifying selection, but there are strong signatures of diversifying selection in new duplicates. In the case of a new duplicate of desat1 in the obscura group species, we show that strong selection on the coding sequence is associated with the evolution of sex-specific expression variation. It seems likely that both sexual selection and ecological adaptation have influenced the evolution of this gene family in Drosophila.     

Patterns of molecular evolution among paralogous floral homeotic genes.

The plant MADS-box regulatory gene family includes several loci that control different aspects of inflorescence and floral development. Orthologs to the Arabidopsis thaliana MADS-box floral meristem genes APETALA1 and CAULIFLOWER and the floral organ identity genes APETALA3 and PISTILLATA were isolated from the congeneric species Arabidopsis lyrata. Analysis of these loci between these two Arabidopsis species, as well as three other more distantly related taxa, reveal contrasting dynamics of molecular evolution between these paralogous floral regulatory genes. Among the four loci, the CAL locus evolves at a significantly faster rate, which may be associated with the evolution of genetic redundancy between CAL and AP1. Moreover, there are significant differences in the distribution of replacement and synonymous substitutions between the functional gene domains of different floral homeotic loci. These results indicate that divergence in developmental function among paralogous members of regulatory gene families is accompanied by changes in rate and pattern of sequence evolution among loci.