Magic traits in speciation: 'magic' but not rare?
TL;DR: It is illustrated that magic traits can be produced by a variety of mechanisms, including ones in which reproductive isolation arises as an automatic by-product of adaptive divergence.
Abstract: Speciation with gene flow is greatly facilitated when traits subject to divergent selection also contribute to non-random mating. Such traits have been called ‘magic traits’, which could be interpreted to imply that they are rare, special, or unrealistic. Here, we question this assumption by illustrating that magic traits can be produced by a variety of mechanisms, including ones in which reproductive isolation arises as an automatic by-product of adaptive divergence. We also draw upon the theoretical literature to explore whether magic traits have a unique role in speciation or can be mimicked in their effects by physically linked trait-complexes. We conclude that magic traits are more frequent than previously perceived, but further work is needed to clarify their importance.
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University of St Andrews1, University of Oldenburg2, Natural History Museum3, Naturalis4, Centre national de la recherche scientifique5, Michigan State University6, University of Lausanne7, University of Wyoming8, Queen Mary University of London9, University of Sheffield10, International Institute for Applied Systems Analysis11, University of Oslo12, University of Vienna13, University of Vermont14, University of East Anglia15, Spanish National Research Council16, University of Cambridge17, University of Konstanz18, University of Zurich19, Royal Botanic Garden Edinburgh20, Harvard University21, Autonomous University of Madrid22, Swiss Federal Institute of Aquatic Science and Technology23, Boston University24, Max Planck Society25, University of Neuchâtel26, University of North Carolina at Chapel Hill27, Lehigh University28, American Museum of Natural History29, University of Montpellier30, University of Liverpool31, Jagiellonian University32, Uppsala University33, German Primate Center34
TL;DR: A perspective on the context and evolutionary significance of hybridization during speciation is offered, highlighting issues of current interest and debate and suggesting that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation.
Abstract: Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near-instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky-Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock-on effects on speciation both within and outside regions of hybridization.
1,715 citations
TL;DR: A comprehensive inventory of the potential implications of personality differences, ranging from population growth and persistence to species interactions and community dynamics, and covering issues such as social evolution, the speed of evolution, evolvability, and speciation is provided.
Abstract: Personality differences are a widespread phenomenon throughout the animal kingdom. Past research has focused on the characterization of such differences and a quest for their proximate and ultimate causation. However, the consequences of these differences for ecology and evolution received much less attention. Here, we strive to fill this gap by providing a comprehensive inventory of the potential implications of personality differences, ranging from population growth and persistence to species interactions and community dynamics, and covering issues such as social evolution, the speed of evolution, evolvability, and speciation. The emerging picture strongly suggests that personality differences matter for ecological and evolutionary processes (and their interaction) and, thus, should be considered a key dimension of ecologically and evolutionarily relevant intraspecific variation.
990 citations
Swiss Federal Institute of Aquatic Science and Technology1, University of Sheffield2, University of Idaho3, Fred Hutchinson Cancer Research Center4, University of Oslo5, École Polytechnique Fédérale de Lausanne6, Umeå University7, University of Lausanne8, Liverpool School of Tropical Medicine9, University of Notre Dame10, ETH Zurich11, University of Copenhagen12, University of Konstanz13, University of Cambridge14, Max Planck Society15, University of Zurich16, University of Groningen17, University of California, Berkeley18, University of British Columbia19, University of Texas at Arlington20
TL;DR: Emergent trends and gaps in understanding are identified, new approaches to more fully integrate genomics into speciation research are proposed, and an integrative definition of the field of speciation genomics is provided.
Abstract: Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.
875 citations
TL;DR: Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time.
Abstract: Most speciation events probably occur gradually, without complete and immediate reproductive isolation, but the full extent of gene flow between diverging species has rarely been characterized on a genome-wide scale. Documenting the extent and timing of admixture between diverging species can clarify the role of geographic isolation in speciation. Here we use new methodology to quantify admixture at different stages of divergence in Heliconius butterflies, based on whole-genome sequences of 31 individuals. Comparisons between sympatric and allopatric populations of H. melpomene, H. cydno, and H. timareta revealed a genome-wide trend of increased shared variation in sympatry, indicative of pervasive interspecific gene flow. Up to 40% of 100-kb genomic windows clustered by geography rather than by species, demonstrating that a very substantial fraction of the genome has been shared between sympatric species. Analyses of genetic variation shared over different time intervals suggested that admixture between these species has continued since early in speciation. Alleles shared between species during recent time intervals displayed higher levels of linkage disequilibrium than those shared over longer time intervals, suggesting that this admixture took place at multiple points during divergence and is probably ongoing. The signal of admixture was significantly reduced around loci controlling divergent wing patterns, as well as throughout the Z chromosome, consistent with strong selection for Mullerian mimicry and with known Z-linked hybrid incompatibility. Overall these results show that species divergence can occur in the face of persistent and genome-wide admixture over long periods of time.
604 citations
Additional excerpts
...Our results imply that the recent focus on mechanisms that permit speciation-with-gene-flow in the literature is not misguided (Servedio et al. 2011; Smadja and Butlin 2011)....
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References
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TL;DR: Measures of directional and stabilizing selection on each of a set of phenotypically correlated characters are derived, retrospective, based on observed changes in the multivariate distribution of characters within a generation, not on the evolutionary response to selection.
Abstract: Natural selection acts on phenotypes, regardless of their genetic basis, and produces immediate phenotypic effects within a generation that can be measured without recourse to principles of heredity or evolution. In contrast, evolutionary response to selection, the genetic change that occurs from one generation to the next, does depend on genetic variation. Animal and plant breeders routinely distinguish phenotypic selection from evolutionary response to selection (Mayo, 1980; Falconer, 1981). Upon making this critical distinction, emphasized by Haldane (1954), precise methods can be formulated for the measurement of phenotypic natural selection. Correlations between characters seriously complicate the measurement of phenotypic selection, because selection on a particular trait produces not only a direct effect on the distribution of that trait in a population, but also produces indirect effects on the distribution of correlated characters. The problem of character correlations has been largely ignored in current methods for measuring natural selection on quantitative traits. Selection has usually been treated as if it acted only on single characters (e.g., Haldane, 1954; Van Valen, 1965a; O'Donald, 1968, 1970; reviewed by Johnson, 1976 Ch. 7). This is obviously a tremendous oversimplification, since natural selection acts on many characters simultaneously and phenotypic correlations between traits are ubiquitous. In an important but neglected paper, Pearson (1903) showed that multivariate statistics could be used to disentangle the direct and indirect effects of selection to determine which traits in a correlated ensemble are the focus of direct selection. Here we extend and generalize Pearson's major results. The purpose of this paper is to derive measures of directional and stabilizing (or disruptive) selection on each of a set of phenotypically correlated characters. The analysis is retrospective, based on observed changes in the multivariate distribution of characters within a generation, not on the evolutionary response to selection. Nevertheless, the measures we propose have a close connection with equations for evolutionary change. Many other commonly used measures of the intensity of selection (such as selective mortality, change in mean fitness, variance in fitness, or estimates of particular forms of fitness functions) have little predictive value in relation to evolutionary change in quantitative traits. To demonstrate the utility of our approach, we analyze selection on four morphological characters in a population of pentatomid bugs during a brief period of high mortality. We also summarize a multivariate selection analysis on nine morphological characters of house sparrows caught in a severe winter storm, using the classic data of Bumpus (1899). Direct observations and measurements of natural selection serve to clarify one of the major factors of evolution. Critiques of the "adaptationist program" (Lewontin, 1978; Gould and Lewontin, 1979) stress that adaptation and selection are often invoked without strong supporting evidence. We suggest quantitative measurements of selection as the best alternative to the fabrication of adaptive scenarios. Our optimism that measurement can replace rhetorical claims for adaptation and selection is founded in the growing success of field workers in their efforts to measure major components of fitness in natural populations (e.g., Thornhill, 1976; Howard, 1979; Downhower and Brown, 1980; Boag and Grant, 1981; Clutton-Brock et
4,990 citations
TL;DR: This work uses multilocus genetics to describe sexual reproduction in an individual-based model and considers the evolution of assortative mating, which leads to reproductive isolation between ecologically diverging subpopulations and conforms well with mounting empirical evidence for the sympatric origin of many species.
Abstract: Understanding speciation is a fundamental biological problem. It is believed that many species originated through allopatric divergence, where new species arise from geographically isolated populations of the same ancestral species. In contrast, the possibility of sympatric speciation (in which new species arise without geographical isolation) has often been dismissed, partly because of theoretical difficulties. Most previous models analysing sympatric speciation concentrated on particular aspects of the problem while neglecting others. Here we present a model that integrates a novel combination of different features and show that sympatric speciation is a likely outcome of competition for resources. We use multilocus genetics to describe sexual reproduction in an individual-based model, and we consider the evolution of assortative mating (where individuals mate preferentially with like individuals) depending either on an ecological character affecting resource use or on a selectively neutral marker trait. In both cases, evolution of assortative mating often leads to reproductive isolation between ecologically diverging subpopulations. When assortative mating depends on a marker trait, and is therefore not directly linked to resource competition, speciation occurs when genetic drift breaks the linkage equilibrium between the marker and the ecological trait. Our theory conforms well with mounting empirical evidence for the sympatric origin of many species.
1,641 citations
1,545 citations
Book•
26 Jul 2004
TL;DR: This book builds for the first time a general, quantitative theory for the origin of species based on the notion of fitness landscapes introduced by Sewall Wright in 1932, generalizing this notion to explore the consequences of the huge dimensionality of Fitness landscapes that correspond to biological systems.
Abstract: The origin of species has fascinated both biologists and the general public since the publication of Darwin's Origin of Species in 1859. Significant progress in understanding the process was achieved in the "modern synthesis," when Theodosius Dobzhansky, Ernst Mayr, and others reconciled Mendelian genetics with Darwin's natural selection. Although evolutionary biologists have developed significant new theory and data about speciation in the years since the modern synthesis, this book represents the first systematic attempt to summarize and generalize what mathematical models tell us about the dynamics of speciation. Fitness Landscapes and the Origin of Species presents both an overview of the forty years of previous theoretical research and the author's new results. Sergey Gavrilets uses a unified framework based on the notion of fitness landscapes introduced by Sewall Wright in 1932, generalizing this notion to explore the consequences of the huge dimensionality of fitness landscapes that correspond to biological systems. In contrast to previous theoretical work, which was based largely on numerical simulations, Gavrilets develops simple mathematical models that allow for analytical investigation and clear interpretation in biological terms. Covering controversial topics, including sympatric speciation and the effects of sexual conflict on speciation, this book builds for the first time a general, quantitative theory for the origin of species.
1,319 citations