The genetic basis of evolution, adaptation and speciation

A primary question in biology concerns the genetic basis of the evolution of novel traits, often in response to environmental changes, and how this can subsequently cause species isolation. This topic was the focus of the symposium on the Genetics of Speciation and Evolution at the annual meeting of the Canadian Society for Ecology and Evolution, held in Banff in May 2011. The presentations revealed some of the rapid advances being made in understanding the genetic basis of adaptation and speciation, as well as the elegant interplay between an organism's genetic complement and the environment that organism experiences.     

Evolutionary community ecology of plant-associated arthropods in terrestrial ecosystems

In the 21st century, researchers have attempted a synthesis between community ecology and evolutionary biology. This emerging research area, which aims to synthesize community ecology and evolutionary biology, is evolutionary community ecology. Evolutionary community ecology addresses how intraspecific trait variation in community members is essential for predicting community properties and, how community properties are a key component of the selective forces that determine genetic and phenotypic variation in a community member. In this paper, I review recent findings in evolutionary community ecology in plant-associated arthropods in terrestrial ecosystems. I discuss roles of both genetic variation and phenotypic plasticity as a source of trait variation in plants in shaping plant-associated arthropod communities. Also, I discuss effects of genetic variation in herbivores on plant-associated arthropod communities. Furthermore, I highlight community context evolution in which multiple species interactions and community composition affect trait evolution of a community member. Finally, I argue that future studies should investigate a feedback loop between community and evolutionary dynamics beyond unidirectional studies on effects of evolution on a community or vice versa. This approach will provide major insights into mechanistic principles for making predictions of community ecology.     

Dualism and conflicts in understanding speciation

Speciation is a central but elusive issue in evolutionary biology. Over the past sixty years, the subject has been studied within a framework conceived by Ernst Mayr and Theodosius Dobzhansky and subsequently developed further by numerous other workers. In this "isolation" theory, the evolution of reproductive isolation is a key element of speciation; natural selection is given only secondary importance while gene flow is considered prohibitive to the process. In this paper, I argue that certain elements in this approach have produced confusion and irreconcilability among students of speciation. The more prominent debates in speciation (i.e., the species definition, sympatry/allopatry, and the role of reinforcement) all derive from an inherent conflict between the "isolation" theory and Darwin's "selection" view on species and speciation (in which disruptive selection is crucial). New data, mainly from field ecology, molecular population genetics, laboratory studies with Drosophila and computer analysis, all suggest that the isolation theory may no longer be the most desirable vantage point from which to explore speciation. Instead, environmental selection in large populations, often unimpeded by ongoing gene flow, appears to be the decisive element. The traditional preoccupation with reproductive isolation has created gaps in our knowledge of several crucial issues, mainly regarding the role of environmental selection and its connection with mate selection.     

Advancing our understanding of the connectivity,evolution and management of marine lobsters through genetics

The genomic revolution has provided powerful insights into the biology and ecology of many non-model organisms. Genetic tools have been increasingly applied to marine lobster research in recent years and have improved our understanding of species delimitation and population connectivity. High resolution genomic markers are just beginning to be applied to lobsters and are now starting to revolutionise our understanding of fine spatial and temporal scales of population connectivity and adaptation to environmental conditions. Lobsters play an important role in the ecosystem and many species are commercially exploited but many aspects of their biology is still largely unknown. Genetics is a powerful tool that can further contribute to our understanding of their ecology and evolution and assist management. Here we illustrate how recent genetic advancements are (1) leading to a step change in our understanding of evolution and adaptation, (2) elucidating factors driving connectivity and recruitment, (3) revealing insights into ecological processes and can (4) potentially revolutionise management of this commercially important group. We discuss how improvements in sequencing technologies and statistical methods for genetic data analyses combined with increased sampling efforts and careful sampling design have transformed our understanding of lobsters biology in recent years. We also highlight possible future directions in the application of genomic tools to lobster research that can aid management, in particular, the close-kin-mark-recapture method. Finally, we identify gaps and challenges in lobster research, such as the lack of any reference genomes and predictions on how lobsters will respond to future environmental conditions.

     

Non-ecological speciation, niche conservatism and thermal adaptation: how are they connected?

During the last decade, the ecological theory of adaptive radiation, and its corollary ??ecological speciation??, has been a major research theme in evolutionary biology. Briefly, this theory states that speciation is mainly or largely the result of divergent selection, arising from niche differences between populations or incipient species. Reproductive isolation evolves either as a result of direct selection on mate preferences (e.g. reinforcement), or as a correlated response to divergent selection (??by-product speciation??). Although there are now many tentative examples of ecological speciation, I argue that ecology??s role in speciation might have been overemphasised and that non-ecological and non-adaptive alternatives should be considered more seriously. Specifically, populations and species of many organisms often show strong evidence of niche conservatism, yet are often highly reproductively isolated from each other. This challenges niche-based ecological speciation and reveals partial decoupling between ecology and reproductive isolation. Furthermore, reproductive isolation might often evolve in allopatry before ecological differentiation between taxa or possibly through learning and antagonistic sexual interactions, either in allopatry or sympatry. Here I discuss recent theoretical and empirical work in this area, with some emphasis on odonates (dragonflies and damselflies) and suggest some future avenues of research. A main message from this paper is that the ecology of species differences is not the same as ecological speciation, just like the genetics of species differences does not equate to the genetics of speciation.     

Sexual imprinting on ecologically divergent traits leads to sexual isolation in sticklebacks

During sexual imprinting, offspring learn parental phenotypes and then select mates who are similar to their parents. Imprinting has been thought to contribute to the process of speciation in only a few rare cases; this is despite imprinting's potential to generate assortative mating and solve the problem of recombination in ecological speciation. If offspring imprint on parental traits under divergent selection, these traits will then be involved in both adaptation and mate preference. Such 'magic traits' easily generate sexual isolation and facilitate speciation. In this study, we show that imprinting occurs in two ecologically divergent stickleback species (benthics and limnetics: Gasterosteus spp.). Cross-fostered females preferred mates of their foster father's species. Furthermore, imprinting is essential for sexual isolation between species; isolation was reduced when females were raised without fathers. Daughters imprinted on father odour and colour during a critical period early in development. These traits have diverged between the species owing to differences in ecology. Therefore, we provide the first evidence that imprinting links ecological adaptation to sexual isolation between species. Our results suggest that imprinting may facilitate the evolution of sexual isolation during ecological speciation, may be especially important in cases of rapid diversification, and thus play an integral role in the generation of biodiversity.     

The ecology of sexual conflict: ecologically dependent parallel evolution of male harm and female resistance in Drosophila melanogaster

The prevalence of sexual conflict in nature, along with the potentially stochastic nature of the resulting coevolutionary trajectories, makes it an important driver of phenotypic divergence and speciation that can operate even in the absence of environmental differences. The majority of empirical work investigating sexual conflict's role in population divergence/speciation has therefore been done in uniform environments and any role of ecology has largely been ignored. However, theory suggests that natural selection can constrain phenotypes influenced by sexual conflict. We use replicate populations of Drosophila melanogaster adapted to alternative environments to test how ecology influences the evolution of male effects on female longevity. The extent to which males reduce female longevity, as well as female resistance to such harm, both evolved in association with adaptation to the different environments. Our results demonstrate that ecology plays a central role in shaping patterns of population divergence in traits under sexual conflict.     

Patterns of thermal adaptation of Bacillus simplex to the microclimatically contrasting slopes of 'Evolution Canyons' I and II, Israel

Identification of selective forces that drive evolution and speciation of bacteria in natural habitats is a central issue in bacterial ecology and evolution. Exploring the adaptive evolution of Bacillus simplex at 'Evolution Canyons' I and II, Israel, we report here on the impact of high heat stress on the speciation progress of individual evolutionary lineages. These canyons represent similar ecological replicates, separated by 40 km, in which the orientation of the sun yields a strong sun-exposed and hot 'African' south-facing slope (SFS) versus a rather cooler and mesic-lush 'European' north-facing slope (NFS) within a distance of only 50-100 m at the bottom and 400 m at the top. Among 131 strains studied, in Luria-Bertani broth, 'African' strains grow better than 'European' strains at a stressful high temperature (43.25 degrees C). The results suggest that adaptation to the hotter and more stressful SFS is continuously ongoing. The patterns of heat adaptation override the phylogenetic history of individual lineages. A positive correlation of growth rates at 43.25 degrees C and 20 degrees C, more markedly among 'African' strains, reflects probably the broader temperature range on the SFS. Summarizing, the hot temperature stress on the 'African' slope is a major environmental force driving the twin evolutionary processes of adaptation and speciation of B. simplex at 'Evolution Canyon'. Finally, we discuss the data in light of current controversies on species concepts.     

Do fitness-equalizing tradeoffs lead to neutral communities?

Neutral theory in ecology is aimed at describing communities where species coexist due to similarities rather than the classically posited niche differences. It assumes that all individuals, regardless of species identity, are demographically equivalent. However, Hubbell suggested that neutral theory may describe even niche communities because tradeoffs equalize fitness across species which differ in their traits. In fact, tradeoffs can involve stabilization as well as fitness equalization, and stabilization involves different dynamics and can lead to different community patterns than neutral theory. Yet the important question remains if neutral theory provides a robust picture of all fitness-equalized communities, of which communities with demographic equivalence are one special case. Here, I examine Hubbell’s suggestion for a purely fitness-equalizing interspecific birth–death tradeoff, expanding neutral theory to a theory describing this broader class of fitness-equalized communities. In particular, I use a flexible framework allowing examination of the influence of speciation dynamics. I find that the scaling of speciation rates with birth and death rates, which is poorly known, has large impacts on community structure. In most cases, the departure from the predictions of current neutral models is substantial. This work suggests that demographic and speciation complexities present a challenge to the future development and use of neutral theory in ecology as null model. The framework presented here will provide a starting point for meeting that challenge, and may also be useful in the development of stochastic niche models with speciation dynamics.     

Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals

Since the time of Charles Darwin, studies of interspecific hybridization have been a major focus for evolutionary biologists. Although this phenomenon has often been viewed as problematic in the fields of ecology, taxonomy and systematics, it has become a primary source of data for studies on speciation and adaptation. Effects from genetic/evolutionary processes, such as recombination and natural selection, usually develop over extended periods of time; however, they are accelerated in cases of hybridization. Interspecific hybrids exhibit novel genomes that are exposed to natural selection, thus providing a key to unravel the ultimate causes of adaptation and speciation. Here we provide firstly a historic perspective of hybridization research, secondly a novel attempt to assess the extent of hybridization among animals and thirdly an overview of the reviews and case studies presented in this theme issue.     

Saccharomyces sensu stricto as a model system for evolution and ecology

Baker's yeast, Saccharomyces cerevisiae, is not only an extensively used model system in genetics and molecular biology, it is an upcoming model for research in ecology and evolution. The available body of knowledge and molecular techniques make yeast ideal for work in areas such as evolutionary and ecological genomics, population genetics, microbial biogeography, community ecology and speciation. As long as ecological information remains scarce for this species, the vast amount of data that is being generated using S. cerevisiae as a model system will remain difficult to interpret in an evolutionary context. Here we review the current knowledge of the evolution and ecology of S. cerevisiae and closely related species in the Saccharomyces sensu stricto group, and suggest future research directions.     

Ephemeral ecological speciation and the latitudinal biodiversity gradient

The richness of biodiversity in the tropics compared to high‐latitude parts of the world forms one of the most globally conspicuous patterns in biology, and yet few hypotheses aim to explain this phenomenon in terms of explicit microevolutionary mechanisms of speciation and extinction. We link population genetic processes of selection and adaptation to speciation and extinction by way of their interaction with environmental factors to drive global scale macroecological patterns. High‐latitude regions are both cradle and grave with respect to species diversification. In particular, we point to a conceptual equivalence of “environmental harshness” and “hard selection” as eco‐evolutionary drivers of local adaptation and ecological speciation. By describing how ecological speciation likely occurs more readily at high latitudes, with such nascent species especially prone to extinction by fusion, we derive the ephemeral ecological speciation hypothesis as an integrative mechanistic explanation for latitudinal gradients in species turnover and the net accumulation of biodiversity.     

Phenotypic integration: studying the ecology and evolution of complex phenotypes

Phenotypic integration refers to the study of complex patterns of covariation among functionally related traits in a given organism. It has been investigated throughout the 20th century, but has only recently risen to the forefront of evolutionary ecological research. In this essay, I identify the reasons for this late flourishing of studies on integration, and discuss some of the major areas of current endeavour: the interplay of adaptation and constraints, the genetic and molecular bases of integration, the role of phenotypic plasticity, macroevolutionary studies of integration, and statistical and conceptual issues in the study of the evolution of complex phenotypes. I then conclude with a brief discussion of what I see as the major future directions of research on phenotypic integration and how they relate to our more general quest for the understanding of phenotypic evolution within the neo‐Darwinian framework. I suggest that studying integration provides a particularly stimulating and truly interdisciplinary convergence of researchers from fields as disparate as molecular genetics, developmental biology, evolutionary ecology, palaeontology and even philosophy of science.     

Rapid response to changing environments during biological invasions: DNA methylation perspectives

Dissecting complex interactions between species and their environments has long been a research hot spot in the fields of ecology and evolutionary biology. The well‐recognized Darwinian evolution has well‐explained long‐term adaptation scenarios; however, “rapid” processes of biological responses to environmental changes remain largely unexplored, particularly molecular mechanisms such as DNA methylation that have recently been proposed to play crucial roles in rapid environmental adaptation. Invasive species, which have capacities to successfully survive rapidly changing environments during biological invasions, provide great opportunities to study molecular mechanisms of rapid environmental adaptation. Here, we used the methylation‐sensitive amplified polymorphism (MSAP) technique in an invasive model ascidian, Ciona savignyi, to investigate how species interact with rapidly changing environments at the whole‐genome level. We detected quite rapid DNA methylation response: significant changes of DNA methylation frequency and epigenetic differentiation between treatment and control groups occurred only after 1 hr of high‐temperature exposure or after 3 hr of low‐salinity challenge. In addition, we detected time‐dependent hemimethylation changes and increased intragroup epigenetic divergence induced by environmental stresses. Interestingly, we found evidence of DNA methylation resilience, as most stress‐induced DNA methylation variation maintained shortly (~48 hr) and quickly returned back to the control levels. Our findings clearly showed that invasive species could rapidly respond to acute environmental changes through DNA methylation modifications, and rapid environmental changes left significant epigenetic signatures at the whole‐genome level. All these results provide fundamental background to deeply investigate the contribution of DNA methylation mechanisms to rapid contemporary environmental adaptation.     

Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species

Evolutionary biologists have often suggested that ecology is important in speciation, in that natural selection may drive adaptive divergence between lineages that inhabit different environments. I suggest that it is the tendency of lineages to maintain their ancestral ecological niche (phylogenetic niche conservatism) and their failure to adapt to new environments which frequently isolates incipient species and begins the process of speciation. Niche conservatism may be an important and widespread component of allopatric speciation but is largely unstudied. The perspective outlined here suggests roles for key microevolutionary processes (i.e., natural selection, adaptation) that are strikingly different from those proposed in previous literature on ecology and speciation. Yet, this perspective is complementary to the traditional view because it focuses on a different temporal stage of the speciation process.     

Taxic evolutionary paleoecology and the ecological context of macroevolutionary change

Summary A traditional focus of evolutionary paleoecology has been the reconstruction of the selective forces that have affected evolving lineages through time. If the history of those lineages is dominated by stasis and punctuation, however, this is at best an inadequate and at worst a misdirected research strategy for macroevolution, because long-term stasis implies that environmental factors may have less influence on evolving lineages than previously believed. Such reasoning has led some proponents of punctuated views to reject ecological interactions as predominant or even significant forces in evolution. This is not a necessary conclusion. It is possible to accept the empirical predominance of stasis in evolution and at the same time the importance of ecology in affecting the course of evolutionary trends within lineages. If stasis prevails, ecology matters in the evolution of lineages if either (1) stabilizing selection is an important cause of stasis or (2) ecological interactions play an important role in controlling the speciation process. Viewing allopatric speciation explicitly as a three-stage process (consisting of formation, persistence and differentiation of isolated populations) clarifies testing of the role of ecology in speciation and may redirect clade-specific evolutionary paleoecology towards more enlightening interaction with other areas of macroevolutionary study.     

The species flocks of lacustrine gastropods: <Emphasis Type="Italic">Tylomelania</Emphasis> on Sulawesi as models in speciation and adaptive radiation

Endemic radiations provide splendid opportunities for studies in evolutionary biology. Species flocks in ancient lakes, such as in Tanganyika, Malawi or Baikal, have featured prominently in evolutionary biology, viewing these “evolutionary theatres” as hotspots of diversification. However, following a century of neglect, the endemic evolution of limnic cerithioidean gastropods in the two central lake systems on the Indonesian island of Sulawesi (i.e. Lake Poso and the lakes of the Malili system, e.g. Danau Matano, Mahalona and Towuti) also provide instructive model cases for the study of speciation mechanisms, adaptive radiation and annidation (i.e. niche exploitation). We here discuss the evolutionary and taxonomic implications of the lacustrine species flocks in Tylomelania from these lakes in Sulawesi as an exceptional endemic assemblage of morphologically distinct viviparous pachychilid gastropods. This first comprehensive compilation of data on both ancient lake systems, Poso and Malili, offers a new perspective on ecological differentiation in this radiation. Presented here within the framework of the theory of evolutionary ecology it provides a research program for acquiring a synthetical perspective that includes morphology, molecular genetics, ecology and biogeography. In this context, it will be possible to compare the species flocks of these truly “Darwinian snails” on Sulawesi with the long enigmatic, so-called thalassoid (i.e. marine-like) gastropod radiation in East African’s Lake Tanganyika.