Rhagoletis pomonella (Diptera: Tephritidae) use volatile compounds emitted from the surface of ripening fruit as important chemosensory cues for recognizing and distinguishing among alternative host plants. Host choice is of evolutionary significance in Rhagoletis because these flies mate on or near the fruit of their respective host plants. Differences in host choice based on fruit odor discrimination therefore result in differential mate choice and prezygotic reproductive isolation, facilitating sympatric speciation in the absence of geographic isolation. We test for a genetic basis for host fruit odor discrimination through an analysis of F2 and backcross hybrids constructed between apple-, hawthorn-, and flowering dogwood-infesting Rhagoletis flies. We recovered a significant proportion (30–65%) of parental apple, hawthorn, and dogwood fly response phenotypes in F2 hybrids, despite the general failure of F1 hybrids to reach odor source spheres. Segregation patterns in F2 and backcross hybrids suggest that only a modest number of allelic differences at a few loci may underlie host fruit odor discrimination. In addition, a strong bias was observed for F2 and backcross flies to orient to the natal fruit blend of their maternal grandmother, implying the existence of cytonuclear gene interactions. We explore the implications of our findings for the evolutionary dynamics of sympatric host race formation and speciation.
Identifying the genetic basis of adaptation is a central goal of evolutionary biology. However, identifying genes and mutations affecting fitness remains challenging because a large number of traits and variants can influence fitness. Selected phenotypes can also be difficult to know a priori, complicating top-down genetic approaches for trait mapping that involve crosses or genome-wide association studies. In such cases, experimental genetic approaches, where one maps fitness directly and attempts to infer the traits involved afterwards, can be valuable. Here, we re-analyse data from a transplant experiment involving Timema stick insects, where five physically clustered single-nucleotide polymorphisms associated with cryptic body coloration were shown to interact to affect survival. Our analysis covers a larger genomic region than past work and revealed a locus previously not identified as associated with survival. This locus resides near a gene, Punch (Pu), involved in pteridine pigments production, implying that it could be associated with an unmeasured coloration trait. However, by combining previous and newly obtained phenotypic data, we show that this trait is not eye or body coloration. We discuss the implications of our results for the discovery of traits, genes and mutations associated with fitness in other systems, as well as for supergene evolution. This article is part of the theme issue 'Genetic basis of adaptation and speciation: from loci to causative mutations'.
Emma L. Berdan1,2, Thomas G. Aubier3,4, Salvatore Cozzolino5, Rui Faria6,7, Jeffrey L. Feder8, Mabel D. Giménez9,10, Mathieu Joron11, Jeremy B. Searle12 and Claire Mérot13 1Department of Marine Sciences, Gothenburg University, Gothenburg 40530, Sweden 2Bioinformatics Core, Department of Biostatistics, Harvard T.H. Chan School of Public Health, Harvard Medical School, Boston, Massachusetts 02115, USA 3Laboratoire Évolution & Diversité Biologique, Université Paul Sabatier Toulouse III, UMR 5174, CNRS/IRD, 31077 Toulouse, France 4Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599, USA 5Department of Biology, University of Naples Federico II, Complesso Universitario di Monte S. Angelo, 80126 Napoli, Italia 6CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO, Laboratório Associado, Universidade do Porto, Vairão, Portugal 7BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, 4485-661 Vairão, Portugal 8Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556, USA 9Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Instituto de Genética Humana de Misiones (IGeHM), Parque de la Salud de la Provincia de Misiones "Dr. Ramón Madariaga," N3300KAZ Posadas, Misiones, Argentina 10Facultad de Ciencias Exactas, Químicas y Naturales, Universidad Nacional de Misiones, N3300LQH Posadas, Misiones, Argentina 11Centre d'Ecologie Fonctionnelle et Evolutive, Université de Montpellier, CNRS, EPHE, IRD, Montpellier, France 12Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853, USA 13CNRS, UMR 6553 Ecobio, OSUR, Université de Rennes, 35000 Rennes, France Correspondence: claire.merot{at}gmail.com; emma.berdan{at}gmail.com
Journal Article THE EFFICACY OF DIVERGENCE HITCHHIKING IN GENERATING GENOMIC ISLANDS DURING ECOLOGICAL SPECIATION Get access Jeffrey L. Feder, Jeffrey L. Feder Dept. of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556Institute for Advanced Study, Wissenschaftskolleg, Berlin, 14193, GermanyE‐mail: feder.2@nd.edu Search for other works by this author on: Oxford Academic Google Scholar Patrik Nosil Patrik Nosil Institute for Advanced Study, Wissenschaftskolleg, Berlin, 14193, GermanyDepartment of Ecology and Evolutionary Biology, University of Boulder Colorado, 80309E‐mail: patrik.nosil@colorado.edu Search for other works by this author on: Oxford Academic Google Scholar Evolution, Volume 64, Issue 6, 1 June 2010, Pages 1729–1747, https://doi.org/10.1111/j.1558-5646.2009.00943.x Published: 01 June 2010 Article history Received: 07 August 2009 Accepted: 09 November 2009 Published: 01 June 2010
Speciation with gene flow is expected to generate a heterogeneous pattern of genomic differentiation. The few genes under or physically linked to loci experiencing strong disruptive selection can diverge, whereas gene flow will homogenize the remainder of the genome, resulting in isolated “genomic islands of speciation.” We conducted an experimental test of this hypothesis in Rhagoletis pomonella , a model for sympatric ecological speciation. Contrary to expectations, we found widespread divergence throughout the Rhagoletis genome, with the majority of loci displaying host differences, latitudinal clines, associations with adult eclosion time, and within-generation responses to selection in a manipulative overwintering experiment. The latter two results, coupled with linkage disequilibrium analyses, provide experimental evidence that divergence was driven by selection on numerous independent genomic regions rather than by genome-wide genetic drift. “Continents” of multiple differentiated loci, rather than isolated islands of divergence, may characterize even the early stages of speciation. Our results also illustrate how these continents can exhibit variable topography, depending on selection strength, availability of preexisting genetic variation, linkage relationships, and genomic features that reduce recombination. For example, the divergence observed throughout the Rhagoletis genome was clearly accentuated in some regions, such as those harboring chromosomal inversions. These results highlight how the individual genes driving speciation can be embedded within an actively diverging genome.
Abstract.— Hybrid zones that result in the genetic assimilation (replacement) of one species by another are underrepresented in the animal literature, most likely due to their transient nature. One such zone involves the rusty crayfish, Orconectes rusticus, and its congener O. propinquus. Orconectes rusticus was recently introduced into northern Wisconsin and Michigan lakes and streams, where it is hybridizing with and displacing resident O. propinquus. Here we report on a study investigating the dynamics of a hybrid zone between the two crayfish in Trout Lake, Wisconsin, where both the time (circa 1979) and location of the initial introduction are known. Our prediction was that hybridization should hasten the demise of O. propinquus because we expected that male O. rusticus (which are larger than congeners) would outcompete male O. propinquus for mates of both species. If hybrid progeny are unfit, then the result would be decreased reproductive output of O. propinquus females. However, we found a pattern of cytonuclear disequilibrium between allozymes and mtDNA suggesting that a majority (94.5%) of F1 hybrids resulted from matings between O. rusticus females and O. propinquus males. Also contrary to expectations, fecundity (O. rusticus and O. propinquus) and early hybrid survivorship did not differ significantly from nonhybrids. Moreover, adults of mixed ancestry were superior to both O. rusticus and O. propinquus in competition for a limiting food resource. Using a single‐locus model, we estimated that hybridization increases the advance of O. rusticus genes in Trout Lake between 4.8% and 36.3% above that due to the previously documented ecological interactions. Consequently, whereas hybridization may be hastening the elimination of genetically pure O. propinquus, introgression is nevertheless slowing the loss of O. propinquus nuclear genes. Although our results suggest that O. rusticus and O. propinquus may not be true species under the biological concept, their ecological differences are of great conservation importance.
Abstract For insect species in temperate environments, seasonal timing is often governed by the regulation of diapause, a complex developmental program that allows insects to weather unfavorable conditions and synchronize their lifecycles with available resources. Diapause consists of a series of phases that govern initiation, maintenance, and termination of this developmental pathway. The evolution of insect seasonal timing depends in part on how these phases of diapause development and post-diapause development interact to affect variation in phenology. Here, we dissect the physiological basis of a recently evolved phenological shift in Rhagoletis pomonella (Diptera: Tephritidae), a model system for ecological divergence. A recently derived population of R. pomonella shifted from specializing on native hawthorn fruit to earlier fruiting introduced apples, resulting in a 3-4 week shift in adult emergence timing. We tracked metabolic rates of individual flies across post-winter development to test which phases of development may act either independently or in combination to contribute to this recently evolved divergence in timing. Apple and hawthorn flies differed in a number of facets of their post-winter developmental trajectories. However, divergent adaptation in adult emergence phenology in these flies was due almost entirely to the end of the pupal diapause maintenance phase, with post-diapause development having a very small effect. The relatively simple underpinnings of variation in adult emergence phenology suggest that further adaptation to seasonal change in these flies for this trait might be largely due to the timing of diapause termination unhindered by strong covariance among different components of post-diapause development. Data accessibility All data (in the form of tables of all metabolic rate measurements for all individual flies in the study) will be available on DRYAD when the manuscript is published.
We established a genetic basis for six newly studied allozyme. in a nondiapausing, laboratory strain of the apple maggot fly, Rhagoletis pomonella, bringing to 18 the number of allozyme loci that have been genetically characterized for this species. We mapped four of the six newly resolved loci to previously known linkage groups. Another locus, Aspartate aminotransferase-1 (Aat-1), was found to be sex-linked and indicated for the first time that males are the heterogametic (XY) sex in R. pomonella. In addition, we observed significant gametic disequilibrium between pairs of linked, nonallelic genes in the laboratory strain. The pattern of linkage disequilibrium for nondiapausing flies was different from that seen in natural populations, suggesting that the laboratory line has become genetically modified during culture.
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