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  • Calboli, Federico C. F.; Byström, Pär; Merilä, Juha (2016)
    Specialization for the use of different resources can lead to ecological speciation. Accordingly, there are numerous examples of ecologically specialized pairs of fish species in postglacial lakes. Using a polymorphic panel of single nucleotide variants, we tested for genetic footprints of within-lake population stratification in nine-spined sticklebacks (Pungitius pungitius) collected from three habitats (viz. littoral, benthic, and pelagic) within a northern Swedish lake. Analyses of admixture, population structure, and relatedness all supported the conclusion that the fish from this lake form a single interbreeding unit.
  • Kahilainen, Kimmo Kalevi; Patterson, William Paul; Sonninen, Eloni; Harrod, Chris; Kiljunen, Mikko (2014)
  • Qvarnstrom, Anna; Alund, Murielle; McFarlane, S. Eryn; Sirkiä, Päivi (2016)
    Climate adaptation is surprisingly rarely reported as a cause for the build-up of reproductive isolation between diverging populations. In this review, we summarize evidence for effects of climate adaptation on pre- and postzygotic isolation between emerging species with a particular focus on pied (Ficedula hypoleuca) and collared (Ficedula albicollis) flycatchers as a model for research on speciation. Effects of climate adaptation on prezygotic isolation or extrinsic selection against hybrids have been documented in several taxa, but the combined action of climate adaptation and sexual selection is particularly well explored in Ficedula flycatchers. There is a general lack of evidence for divergent climate adaptation causing intrinsic postzygotic isolation. However, we argue that the profound effects of divergence in climate adaptation on the whole biochemical machinery of organisms and hence many underlying genes should increase the likelihood of genetic incompatibilities arising as side effects. Fast temperature-dependent co-evolution between mitochondrial and nuclear genomes may be particularly likely to lead to hybrid sterility. Thus, how climate adaptation relates to reproductive isolation is best explored in relation to fast-evolving barriers to gene flow, while more research on later stages of divergence is needed to achieve a complete understanding of climate-driven speciation.
  • Byers, Kelsey J. R. P.; Darragh, Kathy; Fernanda Garza, Sylvia; Abondano Almeida, Diana; Warren, Ian A.; Rastas, Pasi M. A.; Merrill, Richard M.; Schulz, Stefan; McMillan, W. Owen; Jiggins, Chris D. (2021)
    The degree to which loci promoting reproductive isolation cluster in the genome-that is, the genetic architecture of reproductive isolation-can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci. Heliconius butterflies use male sex pheromones to both court females (aphrodisiac wing pheromones) and ward off male courtship (male-transferred antiaphrodisiac genital pheromones), and it is likely that these compounds play a role in reproductive isolation between Heliconius species. Using a set of backcross hybrids between H. melpomene and H. cydno, we investigated the genetic architecture of putative male pheromone compound production. We found a set of 40 significant quantitative trait loci (QTL) representing 33 potential pheromone compounds. QTL clustered significantly on two chromosomes, chromosome 8 for genital compounds and chromosome 20 for wing compounds, and chromosome 20 was enriched for potential pheromone biosynthesis genes. There was minimal overlap between pheromone QTL and known QTL for mate choice and color pattern. Nonetheless, we did detect linkage between a QTL for wing androconial area and optix, a color pattern locus known to play a role in reproductive isolation in these species. This tight clustering of putative pheromone loci might contribute to coincident reproductive isolating barriers, facilitating speciation despite ongoing gene flow.
  • Van Belleghem, Steven M.; Vangestel, Carl; De Wolf, Katrien; De Corte, Zoe; Most, Markus; Rastas, Pasi; De Meester, Luc; Hendrickx, Frederik (2018)
    When environments change, populations may adapt surprisingly fast, repeatedly and even at microgeographic scales. There is increasing evidence that such cases of rapid parallel evolution are fueled by standing genetic variation, but the source of this genetic variation remains poorly understood. In the salt-marsh beetle Pogonus chalceus, short-winged 'tidal' and long-winged 'seasonal' ecotypes have diverged in response to contrasting hydrological regimes and can be repeatedly found along the Atlantic European coast. By analyzing genomic variation across the beetles' distribution, we reveal that alleles selected in the tidal ecotype are spread across the genome and evolved during a singular and, likely, geographically isolated divergence event, within the last 190 Kya. Due to subsequent admixture, the ancient and differentially selected alleles are currently polymorphic in most populations across its range, which could potentially allow for the fast evolution of one ecotype from a small number of random individuals, as low as 5 to 15, from a population of the other ecotype. Our results suggest that cases of fast parallel ecological divergence can be the result of evolution at two different time frames: divergence in the past, followed by repeated selection on the same divergently evolved alleles after admixture. These findings highlight the importance of an ancient and, likely, allopatric divergence event for driving the rate and direction of contemporary fast evolution under gene flow. This mechanism is potentially driven by periods of geographic isolation imposed by large-scale environmental changes such as glacial cycles.
  • Galindo, Juan; Carvalho, Joao; Sotelo, Graciela; Duvetorp, Marten; Costa, Diana; Kemppainen, Petri; Panova, Marina; Kaliontzopoulou, Antigoni; Johannesson, Kerstin; Faria, Rui (2021)
    Low dispersal marine intertidal species facing strong divergent selective pressures associated with steep environmental gradients have a great potential to inform us about local adaptation and reproductive isolation. Among these, gastropods of the genus Littorina offer a unique system to study parallel phenotypic divergence resulting from adaptation to different habitats related with wave exposure. In this study, we focused on two Littorina fabalis ecotypes from Northern European shores and compared patterns of habitat-related phenotypic and genetic divergence across three different geographic levels (local, regional and global). Geometric morphometric analyses revealed that individuals from habitats moderately exposed to waves usually present a larger shell size with a wider aperture than those from sheltered habitats. The phenotypic clustering of L. fabalis by habitat across most locations (mainly in terms of shell size) support an important role of ecology in morphological divergence. A genome scan based on amplified fragment length polymorphisms (AFLPs) revealed a heterogeneous pattern of differentiation across the genome between populations from the two different habitats, suggesting ecotype divergence in the presence of gene flow. The contrasting patterns of genetic structure between nonoutlier and outlier loci, and the decreased sharing of outlier loci with geographic distance among locations are compatible with parallel evolution of phenotypic divergence, with an important contribution of gene flow and/or ancestral variation. In the future, model-based inference studies based on sequence data across the entire genome will help unravelling these evolutionary hypotheses, improving our knowledge about adaptation and its influence on diversification within the marine realm.
  • Konijnendijk, Nellie; Shikano, Takahito; Daneels, Dorien; Volckaert, Filip A. M.; Raeymaekers, Joost A. M. (2015)
    Local adaptation is often obvious when gene flow is impeded, such as observed at large spatial scales and across strong ecological contrasts. However, it becomes less certain at small scales such as between adjacent populations or across weak ecological contrasts, when gene flow is strong. While studies on genomic adaptation tend to focus on the former, less is known about the genomic targets of natural selection in the latter situation. In this study, we investigate genomic adaptation in populations of the three-spined stickleback Gasterosteus aculeatus L. across a small-scale ecological transition with salinities ranging from brackish to fresh. Adaptation to salinity has been repeatedly demonstrated in this species. A genome scan based on 87 microsatellite markers revealed only few signatures of selection, likely owing to the constraints that homogenizing gene flow puts on adaptive divergence. However, the detected loci appear repeatedly as targets of selection in similar studies of genomic adaptation in the three-spined stickleback. We conclude that the signature of genomic selection in the face of strong gene flow is weak, yet detectable. We argue that the range of studies of genomic divergence should be extended to include more systems characterized by limited geographical and ecological isolation, which is often a realistic setting in nature.
  • Thibert-Plante, Xavier; Praebel, Kim; Ostbye, Kjartan; Kahilainen, Kimmo K.; Amundsen, Per-Arne; Gavrilets, Sergey (2020)
    Modern speciation theory has greatly benefited from a variety of simple mathematical models focusing on the conditions and patterns of speciation and diversification in the presence of gene flow. Unfortunately the application of general theoretical concepts and tools to specific ecological systems remains a challenge. Here we apply modeling tools to better understand adaptive divergence of whitefish during the postglacial period in lakes of northern Fennoscandia. These lakes harbor up to three different morphs associated with the three major lake habitats: littoral, pelagic, and profundal. Using large-scale individual-based simulations, we aim to identify factors required for in situ emergence of the pelagic and profundal morphs in lakes initially colonized by the littoral morph. The importance of some of the factors we identify and study - sufficiently large levels of initial genetic variation, size- and habitat-specific mating, sufficiently large carrying capacity of the new niche - is already well recognized. In addition, our model also points to two other factors that have been largely disregarded in theoretical studies: fitness-dependent dispersal and strong predation in the ancestral niche coupled with the lack of it in the new niche(s). We use our theoretical results to speculate about the process of diversification of whitefish in Fennoscandia and to identify potentially profitable directions for future empirical research.