Ecology of a shell convergence between subfamilies of polygyrid land snails

The shell convergence between Neohelix dentifera and Inflectarius ferrissi is an important key to understanding the unusual evolutionary pattern of polygyrid land snails in eastern North America. This group is characterized by conchologically distinct shell-static clades that have radiated ecologically to the extent that shell shape and habitat are not detectably correlated at the species level; furthermore, entire shell-static clades converge conchologically between anatomically distinct lineages (triodopsines and polygyrines). The triodopsine N. dentifera and the polygyrine I. ferrissi both represent unique, drastic shifts from their shell-static clades, and thus are possible founders of new shell-static clades. This study shows that, within a context of high intraspecific variance, N. dentifera and I. ferrissi exhibit ecological parallelism or convergence in addition to conchological convergence. In coarse-grained ecology, both are more associated with acidic, anionic, deep, low- density soils in talus in high-altitude, exposed non-oak-hickory forests than are their close relatives, even though the two are not very close to each other. In fine-grained ecology, N. dentifera converges on I. ferrissi by increased rock-association relative to outgroups, and I. ferrissi likewise converges on N. dentifera by decreased log association. Thus the shell shape unique to these two species appears to be adaptive, whereas their intraspecific ecological variances appear high enough to permit ecological radiation.     

Conceptual bases for quantifying the role of the environment on gene evolution: the participation of positive selection and neutral evolution

To demonstrate that a given change in the environment has contributed to the emergence of a given genotypic and phenotypic shift during the course of evolution, one should ask to what extent such shifts would have occurred without environmental change. Of course, such tests are rarely practical but phenotypic novelties can still be correlated to genomic shifts in response to environmental changes if enough information is available. We surveyed and re-evaluated the published data in order to estimate the role of environmental changes on the course of species and genomic evolution. Only a few published examples clearly demonstrate a causal link between a given environmental change and the fixation of a genomic variant resulting in functional modification (gain, loss or alteration of function). Many others suggested a link between a given phenotypic shift and a given environmental change but failed to identify the underlying genomic determinant(s) and/or the associated functional consequence(s). The proportion of genotypic and phenotypic variation that is fixed concomitantly with environmental changes is often considered adaptive and hence, the result of positive selection, even though alternative causes, such as genetic drift, are rarely investigated. Therefore, the second aim herein is to review evidence for the mechanisms leading to fixation.     

Variation in the rate of convergent evolution: adaptation to a laboratory environment in Drosophila subobscura

Adaptation to novel environments is a central issue in evolutionary biology. One important question is the prevalence of convergence when different populations adapt to the same or similar environments. We investigated this by comparing two studies, 6 years apart, of laboratory adaptation of populations of Drosophila subobscura founded from the same natural location. In both studies several life‐history traits were periodically assayed for the first 14 generations of laboratory adaptation, as well as later generations, and compared with established, laboratory, control populations. The results indicated: (1) a process of convergence for all traits; (2) differences between the two studies in the pattern and rate of convergence; (3) dependence of the evolutionary rates on initial differentiation. The differences between studies might be the result of the differences in the founder populations and/or changes in the lab environment. In either case, the results suggest that microevolution is highly sensitive to genetic and environmental conditions.     

A genome scan of diversifying selection in Ophiocordyceps zombie‐ant fungi suggests a role for enterotoxins in co‐evolution and host specificity

Identification of the genes underlying adaptation sheds light on the biological functions targeted by natural selection. Searches for footprints of positive selection, in the form of rapid amino acid substitutions, and the identification of species‐specific genes have proved to be powerful approaches to identifying the genes involved in host specialization in plant‐pathogenic fungi. We used an evolutionary comparative genomic approach to identify genes underlying host adaptation in the ant‐infecting genus Ophiocordyceps, which manipulates ant behaviour. A comparison of the predicted genes in the genomes of species from three species complexes—O. unilateralis, O. australis and O. subramanianii—revealed an enrichment in pathogenesis‐associated functions, including heat‐labile enterotoxins, among species‐specific genes. Furthermore, these genes were overrepresented among those displaying significant footprints of positive selection. Other categories of genes suspected to be important for virulence and pathogenicity in entomopathogenic fungi (e.g., chitinases, lipases, proteases, core secondary metabolism genes) were much less represented, although a few candidate genes were found to evolve under positive selection. An analysis including orthologs from other entomopathogenic fungi in a broader context showed that positive selection on enterotoxins was specific to the ant‐infecting genus Ophiocordyceps. Together with previous studies reporting the overexpression of an enterotoxin during behavioural manipulation in diseased ants, our findings suggest that heat‐labile enterotoxins are important effectors in host adaptation and co‐evolution in the Ophiocordyceps entomopathogenic fungi.     

Host environment and local genetic adaptation determine phenotype in parasitic Rhinanthus angustifolius

Plants have a remarkable capacity to adapt to local environmental conditions, which can result in ecotypic differentiation. Patterns of differentiation can, however, also be influenced by the extensive phenotypic plasticity exhibited by many plant species. In this study, we evaluated the distinctness of two putative ecotypes of the parasitic herb Rhinanthus angustifolius. We compared population means of characters commonly used to distinguish between the putative ecotypes after growing individuals of R. angustifolius with a variety of host species in a common garden. Resulting data were also pooled over environments to study how phenotypic plasticity affects the distinctness of ecotypes and individual populations. Except for node number, most of the characters were plastic. The pattern of differentiation was consistent with the existence of two, or possibly three, habitat‐related groups of populations; however, we observed considerable overlap in flowering time and morphological characters after pooling data across host environments. The results show that the complex phenological and morphological variation in R. angustifolius is caused by a combination of genetically determined ecotypic differentiation and plastic responses to the host environment and other factors. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2016, 180 , 89–103.     

Divergent population structure and climate associations of a chromosomal inversion polymorphism across the Mimulus guttatus species complex

Chromosomal rearrangement polymorphisms are common and increasingly found to be associated with adaptive ecological divergence and speciation. Rearrangements, such as inversions, reduce recombination in heterozygous individuals and thus can protect favourable allelic combinations at linked loci, facilitating their spread in the presence of gene flow. Recently, we identified a chromosomal inversion polymorphism that contributes to ecological adaptation and reproductive isolation between annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus. Here we evaluate the population genetic structure of this inverted region in comparison with the collinear regions of the genome across the M. guttatus species complex. We tested whether annual and perennial M. guttatus exhibit different patterns of divergence for loci in the inverted and noninverted regions of the genome. We then evaluated whether there are contrasting climate associations with these genomic regions through redundancy analysis. We found that the inversion exhibits broadly different patterns of divergence among annual and perennial M. guttatus and is associated with environmental variation across population accessions. This study is the first widespread population genetic survey of the diversity of the M. guttatus species complex. Our findings contribute to a greater understanding of morphological, ecological, and genetic evolutionary divergence across this highly diverse group of closely related ecotypes and species. Finally, understanding species relationships among M. guttatus sp. has hitherto been stymied by accumulated evidence of substantial gene flow among populations as well as designated species. Nevertheless, our results shed light on these relationships and provide insight into adaptation in life history traits within the complex.     

Testing for adaptation to climate in Arabidopsis thaliana: a calibrated common garden approach

BACKGROUND AND AIMS: A recent method used to test for local adaptation is a common garden experiment where analyses are calibrated to the environmental conditions of the garden. In this study the calibrated common garden approach is used to test for patterns of adaptation to climate in accessions of Arabidopsis thaliana. METHODS: Seedlings from 21 accessions of A. thaliana were planted outdoors in College Park, MD, USA, and development was monitored during the course of a growing season. ANOVA and multiple regression analysis were used to determine if development traits were significant predictors of plant success. Previously published data relating to accessional differences in genetic and physiological characters were also examined. Historical records of climate were used to evaluate whether properties of the site of origin of an accession affected the fitness of plants in a novel environment. KEY RESULTS: By calibrating the analysis to the climatic conditions of the common garden site, performance differences were detected among the accessions consistent with a pattern of adaptation to latitude and climatic conditions. Relatively higher accession fitness was predicted by a latitude and climatic history similar to that of College Park in April and May during the main growth period of this experiment. The climatic histories of the accessions were better predictors of performance than many of the life-history and growth measures taken during the experiment. CONCLUSIONS: It is concluded that the calibrated common garden experiment can detect local adaptation and guide subsequent reciprocal transplant experiments.     

On the logical relationship between natural selection and self-organization

Most evolutionary biologists cherish Darwin's theory of natural selection (NS) as the process of adaptive evolution more than 140 years after publication of his first book on the subject. However, in the past few decades the study of self-organization (SO) in complex dynamical systems has suggested that adaptation may occur through intrinsic reorganization without NS. In this study, we attempt to describe the logical framework that relates the general process of SO to the specific process of NS. We describe NS as a mechanism that coordinates the coevolution of species in an ecosystem to effectively capture, process and dissipate solar energy into the earth's shadow. Finally, we conclude that NS is an emergent process founded on the same thermodynamic imperatives that are thought to underlie all SO. This perspective suggests that the theory of self-organizing systems offers a broader physical context in which to understand the process of NS, rather than contesting it. It even suggests the possibility that there may be a physical basis for understanding the origin of the process of NS. Rather than being merely a fluke of nature, the origin of NS that may be driven by energy flows across gradients.     

Social competition as a driver of phenotype–environment correlations: implications for ecology and evolution

While it is universally recognised that environmental factors can cause phenotypic trait variation via phenotypic plasticity, the extent to which causal processes operate in the reverse direction has received less consideration. In fact individuals are often active agents in determining the environments, and hence the selective regimes, they experience. There are several important mechanisms by which this can occur, including habitat selection and niche construction, that are expected to result in phenotype–environment correlations (i.e. non-random assortment of phenotypes across heterogeneous environments). Here we highlight an additional mechanism – intraspecific competition for preferred environments – that may be widespread, and has implications for phenotypic evolution that are currently underappreciated. Under this mechanism, variation among individuals in traits determining their competitive ability leads to phenotype–environment correlation; more competitive phenotypes are able to acquire better patches. Based on a concise review of the empirical evidence we argue that competition-induced phenotype–environment correlations are likely to be common in natural populations before highlighting the major implications of this for studies of natural selection and microevolution. We focus particularly on two central issues. First, competition-induced phenotype–environment correlation leads to the expectation that positive feedback loops will amplify phenotypic and fitness variation among competing individuals. As a result of being able to acquire a better environment, winners gain more resources and even better phenotypes – at the expense of losers. The distinction between individual quality and environmental quality that is commonly made by researchers in evolutionary ecology thus becomes untenable. Second, if differences among individuals in competitive ability are underpinned by heritable traits, competition results in both genotype–environment correlations and an expectation of indirect genetic effects (IGEs) on resource-dependent life-history traits. Theory tells us that these IGEs will act as (partial) constraints, reducing the amount of genetic variance available to facilitate evolutionary adaptation. Failure to recognise this will lead to systematic overestimation of the adaptive potential of populations. To understand the importance of these issues for ecological and evolutionary processes in natural populations we therefore need to identify and quantify competition-induced phenotype–environment correlations in our study systems. We conclude that both fundamental and applied research will benefit from an improved understanding of when and how social competition causes non-random distribution of phenotypes, and genotypes, across heterogeneous environments.     

Evaluating the role of natural selection in the evolution of gene regulation

Surveys of gene expression reveal extensive variability both within and between a wide range of species. Compelling cases have been made for adaptive changes in gene regulation, but the proportion of expression divergence attributable to natural selection remains unclear. Distinguishing adaptive changes driven by positive selection from neutral divergence resulting from mutation and genetic drift is critical for understanding the evolution of gene expression. Here, we review the various methods that have been used to test for signs of selection in genomic expression data. We also discuss properties of regulatory systems relevant to neutral models of gene expression. Despite some potential caveats, published studies provide considerable evidence for adaptive changes in gene expression. Future challenges for studies of regulatory evolution will be to quantify the frequency of adaptive changes, identify the genetic basis of expression divergence and associate changes in gene expression with specific organismal phenotypes.     

Stay in shape: Assessing the adaptive potential of shell morphology and its sensitivity to temperature in the invasive New Zealand mud snail Potamopyrgus antipodarum through phenotypic plasticity and natural selection in Europe

Climate change may force organisms to adapt genetically or plastically to new environmental conditions. Invasive species show remarkable potential for rapid adaptation. The ovoviviparous New Zealand mud snail (NZMS), Potamopyrgus antipodarum, has successfully established across Europe with two clonally reproducing mitochondrial lineages since its arrival in the first half of the 19th century. Its remarkable variation in shell morphology was shown to be fitness relevant. We investigated the effects of temperature on shell morphology across 11 populations from Germany and the Iberian Peninsula in a common garden across three temperatures. We analyzed size and shape using geometric morphometrics. For both, we compared reaction norms and estimated heritabilities. For size, the interaction of temperature and haplotype explained about 50% of the total variance. We also observed more genotype by environment interactions indicating a higher degree of population differentiation than in shape. Across the three temperatures, size followed the expectations of the temperature‐size rule, with individuals growing larger in cold environments. Changes in shape may have compensated for changes in size affecting space for brooding embryos. Heritability estimates were relatively high. As indicated by the very low coefficients of variation for clonal repeatability (CV _A ), they can probably not be compared in absolute terms. However, they showed some sensitivity to temperature, in haplotype t more so than in z, which was only found in Portugal. The low CV _A values indicate that genetic variation among European populations is still restricted with a low potential to react to selection. A considerable fraction of the genetic variation was due to differences between the clonal lineages. The NZMS has apparently not been long enough in Europe to accumulate significant genetic variation relevant for morphological adaptation. As temperature is obviously not the sole factor influencing shell morphology, their interaction will probably not be a factor limiting population persistence under a warming climate in Europe.     

Interactions between sexual and natural selection on the evolution of a plumage badge

The evolutionary stability of signals varies due to interactions between sexual and natural selection. A tidal-marsh sparrow, Melospiza georgiana nigrescens, possesses darker pigmentation than an inland-marsh sparrow, M. g. georgiana. Studies of feather-degrading bacteria and convergent evolution among salt-marsh vertebrates suggest this dark coloration is due to environmental selection. Sexually dichromatic swamp sparrow crowns, however, may be additionally under sexual selection. We investigated ties between two plumage patches (rusty cap and black forehead) and two behaviors (male-male aggression and parental care) in the coastal and inland subspecies to test the effect of sexual versus natural selection on badge evolution. Across both subspecies the extent of rusty feathers in the cap patch was correlated positively with parental care and negatively with aggression, and the extent of black feathers in the forehead patch was correlated positively with aggression. Males with larger forehead patches produced more offspring along the coast, while males with larger cap patches did so inland. The date of the first nesting attempt for both subspecies correlated with cap patch extent, suggesting a similar role for female choice. Natural selection likely accounts for darker coastal females. Coastal male head color, however, is darker due to increased selection for larger forehead patches via intrasexual competition, yet it remains largely rusty due to female choice for larger cap patches. Increased sexual dichromatism among coastal plain swamp sparrows thus provides a clear example of the interplay between sexual and natural selection in subspecies divergence.     

UNVEILing connections between genotype,phenotype, and fitness in natural populations

Understanding the links between genetic variation and fitness in natural populations is a central goal of evolutionary genetics. This monumental task spans the fields of classical and molecular genetics, population genetics, biochemistry, physiology, developmental biology, and ecology. Advances to our molecular and developmental toolkits are facilitating integrative approaches across these traditionally separate fields, providing a more complete picture of the genotype‐phenotype map in natural and non‐model systems. Here, we summarize research presented at the first annual symposium of the UNVEIL Network, an NSF‐funded collaboration between the University of Montana and the University of Nebraska, Lincoln, which took place from the 1st to the 3rd of June, 2018. We discuss how this body of work advances basic evolutionary science, what it implies for our ability to predict evolutionary change, and how it might inform novel conservation strategies.     

Testing the role of ecological selection on colour pattern variation in the butterfly Parnassius clodius

Colour pattern has served as an important phenotype in understanding the process of natural selection, particularly in brightly coloured and variable species like butterflies. However, different selective forces operate on aspects of colour pattern, for example by favouring warning colours in eyespots or alternatively favoring investment in thermoregulatory properties of melanin. Additionally, genetic drift influences colour phenotypes, especially in populations undergoing population size change. Here, we investigated the relative roles of genetic drift and ecological selection in generating the phenotypic diversity of the butterfly Parnassius clodius. Genome‐wide patterns of single nucleotide polymorphism data show that P. clodius forms three population clusters, which experienced a period of population expansion following the last glacial maximum and have since remained relatively stable in size. After correcting for relatedness, morphological variation is best explained by climatic predictor variables, suggesting ecological selection generates trait variability. Solar radiation and precipitation are both negatively correlated with increasing total melanin in both sexes, supporting a thermoregulatory function of melanin. Similarly, wing size traits are significantly larger in warmer habitats for both sexes, supporting a Converse Bergmann Rule pattern. Bright red coloration is negatively correlated with temperature seasonality and solar radiation in males, and weakly associated with insectivorous avian predators in univariate models, providing mixed evidence that selection is linked to warning coloration and predator avoidance. Together, these results suggest that elements of butterfly wing phenotypes respond independently to different sources of selection and that thermoregulation is an important driver of phenotypic differentiation in Parnassian butterflies.     

An exact form of the breeder's equation for the evolution of a quantitative trait under natural selection

Starting with the Price equation, I show that the total evolutionary change in mean phenotype that occurs in the presence of fitness variation can be partitioned exactly into five components representing logically distinct processes. One component is the linear response to selection, as represented by the breeder's equation of quantitative genetics, but with heritability defined as the linear regression coefficient of mean offspring phenotype on parent phenotype. The other components are identified as constitutive transmission bias, two types of induced transmission bias, and a spurious response to selection caused by a covariance between parental fitness and offspring phenotype that cannot be predicted from parental phenotypes. The partitioning can be accomplished in two ways, one with heritability measured before (in the absence of) selection, and the other with heritability measured after (in the presence of) selection. Measuring heritability after selection, though unconventional, yields a representation for the linear response to selection that is most consistent with Darwinian evolution by natural selection because the response to selection is determined by the reproductive features of the selected group, not of the parent population as a whole. The analysis of an explicitly Mendelian model shows that the relative contributions of the five terms to the total evolutionary change depends on the level of organization (gene, individual, or mated pair) at which the parent population is divided into phenotypes, with each frame of reference providing unique insight. It is shown that all five components of phenotypic evolution will generally have nonzero values as a result of various combinations of the normal features of Mendelian populations, including biparental sex, allelic dominance, inbreeding, epistasis, linkage disequilibrium, and environmental covariances between traits. Additive genetic variance can be a poor predictor of the adaptive response to selection in these models. The narrow-sense heritability sigma2A/sigma2P should be viewed as an approximation to the offspring-parent linear regression rather than the other way around.     

Exploring the interplay between natural and intersexual selection on the evolution of a cognitive trait

There has been an increased focus on the role of natural and sexual selection in shaping cognitive abilities, but the importance of the interaction between both forces remains largely unknown. Intersexual selection through female mate choice might be an important driver of the evolution of cognitive traits, especially in monogamous species, where females may obtain direct fitness benefits by choosing mates with better cognitive abilities. However, the importance given by female to male cognitive traits might vary among species and/or populations according to their life‐history traits and ecology. To disentangle the effects of natural and sexual selection, here we use an agent‐based simulation model and compare the model''s predictions when females mate with the first randomly encountered male (i.e., under natural selection) versus when they choose among males based on their cognitive trait values (i.e., under natural and intersexual selection). Males and females are characterized, respectively, by their problem‐solving ability and assessment strategy. At each generation, agents go through (1) a choosing phase during which females assess the cognitive abilities of potential mates until eventually finding an acceptable one and (2) a reproductive phase during which all males compete for limited resources that are exploited at a rate, which depends on their cognitive abilities. Because males provide paternal care, the foraging success of mated males determines the breeding success of the pair through its effect on nestling provisioning efficiency. The model predicts that intersexual selection plays a major role in most ecological conditions, by either reinforcing or acting against the effect of natural selection. The latter case occurs under harsh environmental conditions, where intersexual selection contributes to maintaining cognitive diversity. Our findings thus demonstrate the importance of considering the interaction between both selective forces and highlight the need to build a conceptual framework to target relevant cognitive traits.     

Improved genome assembly of Chinese shrimp (Fenneropenaeus chinensis) suggests adaptation to the environment during evolution and domestication

A high-quality reference genome is necessary to determine the molecular mechanisms underlying important biological phenomena; therefore, in the present study, a chromosome-level genome assembly of the Chinese shrimp Fenneropenaeus chinensis was performed. Muscle of a male shrimp was sequenced using PacBio platform, and assembled by Hi-C technology. The assembled F. chinensis genome was 1.47 Gb with contig N50 of 472.84 Kb, including 57.73% repetitive sequences, and was anchored to 43 pseudochromosomes, with scaffold N50 of 36.87 Mb. In total, 25,026 protein-coding genes were predicted. The genome size of F. chinensis showed significant contraction in comparison with that of other penaeid species, which is likely related to migration observed in this species. However, the F. chinensis genome included several expanded gene families related to cellular processes and metabolic processes, and the contracted gene families were associated with virus infection process. The findings signify the adaptation of F. chinensis to the selection pressure of migration and cold environment. Furthermore, the selection signature analysis identified genes associated with metabolism, phototransduction, and nervous system in cultured shrimps when compared with wild population, indicating targeted, artificial selection of growth, vision, and behavior during domestication. The construction of the genome of F. chinensis provided valuable information for the further genetic mechanism analysis of important biological processes, and will facilitate the research of genetic changes during evolution.     

Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations

Understanding the genetic basis of local adaptation requires insight in the fitness effects of individual loci under natural field conditions. While rapid progress is made in the search for genes that control differences between plant populations, it is typically unknown whether the genes under study are in fact key targets of habitat-specific natural selection. Using a quantitative trait loci (QTL) approach, we show that a QTL associated with flowering-time variation between two locally adapted wild barley populations is an important determinant of fitness in one, but not in the other population's native habitat. The QTL mapped to the same position as a habitat-specific QTL for field fitness that affected plant reproductive output in only one of the parental habitats, indicating that the genomic region is under differential selection between the native habitats. Consistent with the QTL results, phenotypic selection of flowering time differed between the two environments, whereas other traits (growth rate and seed weight) were under selection but experienced no habitat-specific differential selection. This implies the flowering-time QTL as a driver of adaptive population divergence. Our results from phenotypic selection and QTL analysis are consistent with local adaptation without genetic trade-offs in performance across environments, i.e. without alleles or traits having opposing fitness effects in contrasting environments.