Resource-based adaptive divergence in the freshwater fish Telmatherina from Lake Matano, Indonesia

Adaptive radiations are an important source of biodiversity, but resolving which ecological pressures seed these processes in natural systems remains difficult. Here the adaptive radiation among Telmatherina, a genus of freshwater fish endemic to an ancient lake in central Sulawesi, Indonesia, was examined to determine its causal root. We demonstrate that all Telmatherina in this lake can be categorized into three lineages each possessing specialized skull shapes and pharyngeal jaw bones allowing them to exploit different resources. These data demonstrate a natural example of how resource partitioning has likely initiated adaptive radiation in a resource limited environment.     

Body shape vs. colour associated initial divergence in the Telmatherina radiation in Lake Matano, Sulawesi, Indonesia

Highly polymorphic colouration patterns are often associated with sexual selection in fish and can be the initial cause of divergence among closely related taxa. Here we use genetic, body colour and geometric morphometric data collected on 118 fish from Lake Matano, Sulawesi, Indonesia to test if colouration is the initial cause of divergence in the radiating Telmatherina genus. Results reveal that all Telmatherina previously described in this system can be categorized into three mitochondrial lineages and that colouration is only weakly associated with early divergence. Clade-specific body shapes, however, likely adapted to microenvironments are key to the initial divergence in this system. Data also show that although colourations were not likely instrumental in seeding divergence in these fish, they appear to have developed in parallel within each clade. Our results are consistent with an emerging pattern repeated in many vertebrate radiations, whereby divergence by colouration or other display traits is preceded by specialization to environmental adaptive peaks.     

The genetic architecture of ecological speciation and the association with signatures of selection in natural lake whitefish (Coregonus sp. Salmonidae) species pairs

Adaptive evolutionary change is contingent on variation and selection; thus, understanding adaptive divergence and ultimately speciation requires information on both the genetic basis of adaptive traits as well as an understanding of the role of divergent natural selection on those traits. The lake whitefish (Coregonus clupeaformis) consists of several sympatric "dwarf" (limnetic) and normal (benthic) species pairs that co-inhabit northern postglacial lakes. These young species pairs have evolved independently and display parallelism in life history, behavioral, and morphological divergence associated with the use of distinct trophic resources. We identified phenotype-environment associations and determined the genetic architecture and the role of selection modulating population genetic divergence in sympatric dwarf and normal lake whitefish. The genetic architecture of 9 adaptive traits was analyzed in 2 hybrid backcrosses individually phenotyped throughout their life history. Significant quantitative trait loci (QTL) were associated with swimming behavior (habitat selection and predator avoidance), growth rate, morphology (condition factor and gill rakers), and life history (onset of maturity and fecundity). Genome scans among 4 natural sympatric pairs, using loci segregating in the map, revealed a signature of selection for 24 loci. Loci exhibiting a signature of selection were associated with QTL relative to other regions of the genome more often than expected by chance alone. Two parallel QTL outliers for growth and condition factor exhibited segregation distortion in both mapping families, supporting the hypothesis that adaptive divergence contributing to parallel reductions of gene flow among natural populations may cause genetic incompatibilities. Overall, these findings offer evidence that the genetic architecture of ecological speciation is associated with signatures of selection in nature, providing strong support for the hypothesis that divergent natural selection is currently maintaining adaptive differentiation and promoting ecological speciation in lake whitefish species pairs.     

Diversifying selection drives parallel evolution of gill raker number and body size along the speciation continuum of European whitefish

Adaptive radiation is the evolution of ecological and phenotypical diversity. It arises via ecological opportunity that promotes the exploration of underutilized or novel niches mediating specialization and reproductive isolation. The assumed precondition for rapid local adaptation is diversifying natural selection, but random genetic drift could also be a major driver of this process. We used 27 populations of European whitefish (Coregonus lavaretus) from nine lakes distributed in three neighboring subarctic watercourses in northern Fennoscandia as a model to test the importance of random drift versus diversifying natural selection for parallel evolution of adaptive phenotypic traits. We contrasted variation for two key adaptive phenotypic traits correlated with resource utilization of polymorphic fish; the number of gill rakers and the total length of fish, with the posterior distribution of neutral genetic differentiation from 13 microsatellite loci, to test whether the observed phenotypic divergence could be achieved by random genetic drift alone. Our results show that both traits have been under diversifying selection and that the evolution of these morphs has been driven by isolation through habitat adaptations. We conclude that diversifying selection acting on gill raker number and body size has played a significant role in the ongoing adaptive radiation of European whitefish morphs in this region.     

Genomic architecture of habitat‐related divergence and signature of directional selection in the body shapes of Gnathopogon fishes

Evolution of ecomorphologically relevant traits such as body shapes is important to colonize and persist in a novel environment. Habitat‐related adaptive divergence of these traits is therefore common among animals. We studied the genomic architecture of habitat‐related divergence in the body shape of Gnathopogon fishes, a novel example of lake–stream ecomorphological divergence, and tested for the action of directional selection on body shape differentiation. Compared to stream‐dwelling Gnathopogon elongatus, the sister species Gnathopogon caerulescens, exclusively inhabiting a large ancient lake, had an elongated body, increased proportion of the caudal region and small head, which would be advantageous in the limnetic environment. Using an F₂ interspecific cross between the two Gnathopogon species (195 individuals), quantitative trait locus (QTL) analysis with geometric morphometric quantification of body shape and restriction‐site associated DNA sequencing‐derived markers (1622 loci) identified 26 significant QTLs associated with the interspecific differences of body shape‐related traits. These QTLs had small to moderate effects, supporting polygenic inheritance of the body shape‐related traits. Each QTL was mostly located on different genomic regions, while colocalized QTLs were detected for some ecomorphologically relevant traits that are proxy of body and caudal peduncle depths, suggesting different degree of modularity among traits. The directions of the body shape QTLs were mostly consistent with the interspecific difference, and QTL sign test suggested a genetic signature of directional selection in the body shape divergence. Thus, we successfully elucidated the genomic architecture underlying the adaptive changes of the quantitative and complex morphological trait in a novel system.     

Generic scan using AFLP markers as a means to assess the role of directional selection in the divergence of sympatric whitefish ecotypes

Under the ecological theory of adaptive radiation, adaptation and reproductive isolation are thought to evolve as a result of divergent natural selection. Accordingly, elucidating the genetic basis of these processes is essential toward understanding the role of selection in shaping biological diversity. In this respect, the number of genes that evolved by selection remains contentious. To address this issue, the pattern of genetic differentiation obtained using 440 AFLP loci was compared with that expected under neutrality in four sympatric pairs of lake whitefish ecotypes that evolved adaptive phenotypic differences associated with the exploitation of distinct ecological niches. On average, 14 loci showed restricted gene flow relative to neutral expectation, suggesting a role of directional selection on their divergence. Among all loci that are most likely under directional selection, six exhibited parallel patterns of divergence, which provided further support for the role of selection in driving their divergence. Overall, these results indicate that only a small proportion of scored AFLP loci (between 1.4% and 3.2%) might be linked to genes implicated in the adaptive radiation of lake whitefish.     

Quantitative trait and allozyme divergence in the Greenfinch (Carduelis chloris, Aves: Fringillidae)

Quantitative trait divergence and variability among 12 greenfinch populations across continental Europe was examined and compared to divergence in neutral genetic markers (allozymes). The added among locality variance component for 16 skeletal traits was large (mean 28%, range 4–48%) equalling a divergence of up to three SD units. The divergence in quantitative traits (Qst = 0.04-0.48) greatly exceeded that in alloymes (F_ST= 0.01-0.07), indicating the differentiation in quantitative traits to be larger than expected by mutation and drift alone. This conclusion was consistent also with results from the multivariate approach of Rogers & Harpending. However, genetic and morphometric distances between populations were positively correlated, even when controlling for the geographic distance separating pairs of populations. In concordance with Bergmann's rule, most traits were strongly and positively correlated with latitude, indicating latitudinally ordered genetic or/and environmental effects. However, the correlation between lower mandible width and latitude was strongly negative, demonstrating an inverse relationship between beak size and body size across the populations. These results are interpreted to reflect the re-colonization of history of northern Europe (genetic and geographic distances correlated) which has been paralleled by selection acting on quantitative traits (Q_ST>F_ST)- In particular, the counter-gradient variation in beak width, a functionally important trait, is suggestive of an adaptive basis for quantitative trait divergence.     

CORRELATED TROPHIC SPECIALIZATION AND GENETIC DIVERGENCE IN SYMPATRIC LAKE WHITEFISH ECOTYPES (COREGONUS CLUPEAFORMIS): SUPPORT FOR THE ECOLOGICAL SPECIATION HYPOTHESIS

There is ample empirical evidence that phenotypic diversification in an adaptive radiation is the outcome of divergent natural selection related to differential resource use. In contrast, the role of ecological forces in favoring and maintaining reproductive isolation in nature remains poorly understood. If the same forces driving phenotypic divergence are also responsible for speciation, one would predict a correlation between the extent of trophic specialization (reflecting variable intensity of divergent natural selection) and that of reproductive isolation being reached in a given environment. We tested this hypothesis by comparing the extent of morphological and genetic differentiation between sympatric dwarf and normal whitefish ecotypes (Coregonus sp.) from six lakes of the St. John River basin (eastern Canada and northern Maine). Eight meristic variables, 19 morphometric variables, and six microsatellite loci were used to quantify morphological and genetic differentiation, respectively. Dwarf and normal ecotypes in each lake differed primarily by traits related to trophic specialization, but the extent of differentiation varied among lakes. Significant but variable genetic divergence between ecotypes within lakes was also observed. A negative correlation was observed between the extent of gene flow between ecotypes within a lake and that of their morphological differentiation in trophic-related traits. The extent of reproductive isolation reached between dwarf and normal whitefish ecotypes appears to be driven by the potential for occupying distinct trophic niches and, thus, by the same selective forces driving tropic specialization in each lake. These results therefore support the hypothesis of ecological speciation.     

Contrasting modes of natural selection acting on pigmentation genes in the Drosophila dunni subgroup

Genes that encode for divergent adaptive traits may have genealogies that contrast with those from loci that are not functionally involved in differentiation. Here, we examine DNA sequence variation among the species of the eastern Caribbean Drosophila dunni subgroup at two loci, yellow and dopa decaboxylase (Ddc), which both play integral roles in pigmentation patterning of adult Drosophila. Phylogenetic analyses of these loci produce gene genealogies with topologies that mirror those described for other nuclear genes: the six morphologically distinct species within the subgroup are divided into only three lineages, with one lineage containing four species that share extensive ancestral polymorphism. At the Ddc locus these major lineages are delineated only by silent site variation. We observe a significantly higher rate of synonymous site divergence than non-synonymous divergence, consistent with strong purifying selection acting on the locus. In contrast, the yellow locus exhibits patterns of amino acid divergence and nucleotide diversity that are consistent with recent diversifying selection acting in two different lineages. This selection appears to be targeting amino acid variants in the signal sequence of the Yellow protein, a region which is tightly constrained among members of the larger D. cardini radiation. This result highlights not only the potential importance of yellow in the evolution of divergent pigmentation patterns among members of the D. dunni subgroup, but also hints that variation in signal peptide sequences may play a role in phenotypic diversification.     

Quantitative genetics of yield breeding forPopulus short rotation culture. III. Efficiency of indirect selection on tree geometry

Quantitative analysis of genetic covariances was used to identify the critical morphological components of wood productivity and to evaluate the efficiency of indirect selection for these components at the four levels of biological organization, (1) leaf, (2) branch, (3) main stem, and (4) whole-tree, in 4-yearPopulus deltoides ×P. simonii andP. deltoides ×P. nigra F₁ progeny. A total of 44 morphometric traits measured at the four organizational levels showed varying genetic associations with productivity, variations being dependent on traits, developmental processes (current terminal, sylleptics, and proleptics), and hybridization combinations. Most of the leaf and branch traits on the current terminal and/or sylleptic branches had higher genetic correlations with stem-wood volume than those on proleptics, which resulted in larger indirect selection responses in volume, especially in DxS progeny. Indirect clonal selection on leaf size and area, branching capacity, and branch angle at age 4 years was expected to generate 10–35% more genetic gain per year in 6-year volume than direct selection on 6-year volume in the DxS progeny. The efficiency of indirect selection on the numbers of different order branches and bifurcation ratio was greater than 1.0 relative to that for direct selection for stemwood volume in the D × N progeny. Under the pressure of artificial selection for superior volume production, with the proportion selected=15%, the two F₁ progeny populations exhibited distinct evolutionary divergence in tree geometry. The high-yielding D × S clones displayed a decurrent-like crown with strong apical dominance, whereas the crown ideotype for the high-yielding D × N clones was found to be excurrent-like and surrounded by dense foliage and branches.     

Genetically based phenotype-environment association for swimming behavior in lake whitefish ecotypes (Coregonus clupeaformis Mitchill)

Abstract.— Studies of phenotype-environment associations in adaptive radiation have focused largely on morphological traits related to resource-based phenotypic differences. The genetic basis of adaptive behaviors implicated in population divergence remains poorly understood, as few studies have tested the hypothesis of behavioral phenotype-environment associations. We provide evidence of a phenotype-environment association for differential adaptive swimming behaviors through experiments conducted on dwarf, normal, and hybrid lake whitefish ( Coregonus clupeaformis ). Highly significant differences were observed for depth selection, directional changes, and burst swimming, implicating a genetic basis for these behaviors. Hybrid crosses revealed that depth selection is under additive genetic control, while dominance effects were suggested for directional changes and burst swimming. Estimates for the genetic basis of behavioral differentiation from an animal model were consistent with these observations. Comparative estimates of behavioral differentiation ( Q _ST) against neutral expectations ( F _ST) revealed pronounced departures from neutral expectations in all three behavioral phenotypes, consistent with the hypothesis that directional selection has driven the divergence of behavior in dwarf and normal lake whitefish ecotypes.     

Gene flow in Dubautia arborea and D. ciliolata: the roles of ecology and isolation by distance in maintaining species boundaries despite ongoing hybridization

The relative roles of gene flow and natural selection in maintaining species differentiation have been a subject of debate for some time. The traditional view is that gene flow constrains adaptive divergence and maintains species cohesiveness. Alternatively, ecological speciation posits that the reverse is true: that adaptive ecological differentiation constrains gene flow. In this study, we examine gene flow and population differentiation among populations of two species of the Hawaiian silversword alliance, Dubautia arborea and D. ciliolata. We compare divergence in putatively neutral microsatellite markers with divergence in leaf morphometric traits, which may be selectively important or physiologically linked to selectively important traits. Gene flow between populations was found to be significant in only one of the two species, D. arborea. Leaf morphometric differentiation between species was significant, though not among populations within species. No evidence of effective genetic introgression was observed between apparently 'pure' populations of these species. Gene flow as measured by microsatellites was not correlated with geographic distance between populations, but was correlated with the linear placement of the widest part of the leaf. Because these two species are interfertile, as demonstrated by the presence of active hybrid zone, the lack of genetic introgression and the maintenance of species boundaries may be associated with natural selection on differential habitat.     

Morphological variation in a secondary contact between divergent lineages of brown trout (Salmo trutta) from the Iberian Peninsula

The aim of this study was to analyze the morphological variation of brown trout (Salmo trutta) in the Duero basin, an Atlantic river basin in the Iberian Peninsula, where a spatial segregation of two divergent lineages was previously reported, based on isozyme, microsatellite and mtDNA data. In these studies, two divergent pure regions (Pisuerga and Lower-course) and several hybrid populations between them were identified. Morphological variation was evaluated in 11 populations representative of the genetic differentiation previously observed in the Duero basin, using multivariate analysis on 12 morphometric and 4 meristic traits. A large differentiation between populations was observed (interpopulation component of variance: 41.8%), similar to that previously detected with allozymes and microsatellites. Morphometric differentiation was also reflected by the high classification success of pure and hybrid individuals to their respective populations, using multivariate discriminant functions (94.1% and 79.0%, respectively). All multivariate and clustering analyses performed demonstrated a strong differentiation between the pure regions. The hybrid populations, though showing large differentiation among them, evidenced an intermediate position between the pure samples. Head and body shape traits were the most discriminant among the morphometric characters, while pectoral rays and gillrakers were the most discriminant among the meristic traits. These results confirmed the high divergence of the brown trout from the Duero basin and suggest some traits on which selection could be acting to explain the spatial segregation observed.     

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.     

PHENOTYPE-DEPENDENT NATIVE HABITAT PREFERENCE FACILITATES DIVERGENCE BETWEEN PARAPATRIC LAKE AND STREAM STICKLEBACK

Adaptive divergence between adjoining populations reflects a balance between the diversifying effect of divergent selection and the potentially homogenizing effect of gene flow. In most models of migration-selection balance, gene flow is assumed to reflect individuals' inherent capacity to disperse, without regard to the match between individuals' phenotypes and the available habitats. However, habitat preferences can reduce dispersal between contrasting habitats, thereby alleviating migration load and facilitating adaptive divergence. We tested whether habitat preferences contribute to adaptive divergence in a classic example of migration-selection balance: parapatric lake and stream populations of three-spine stickleback ( Gasterosteus aculeatus ). Using a mark-transplant-recapture experiment on morphologically divergent parapatric populations, we showed that 90% of lake and stream stickleback returned to their native habitat, reducing migration between habitats by 76%. Furthermore, we found that dispersal into a nonnative habitat was phenotype dependent. Stream fish moving into the lake were morphologically more lake-like than those returning to the stream (and the converse for lake fish entering the stream). The strong native habitat preference documented here increases the extent of adaptive divergence between populations two- to fivefold relative to expectations with random movement. These results illustrate the potential importance of adaptive habitat choice in driving parapatric divergence.     

Evolutionary diversification of opercle shape in Cook Inlet threespine stickleback

We investigated the evolution of a large facial bone, the opercle (OP), in lake populations of the threespine stickleback that were founded by anadromous ancestors, in Cook Inlet, Alaska. Recent studies characterized OP variation among marine and lake populations and mapped a quantitative trait locus with a large influence on OP shape. Using populations from diverse environments and independent evolutionary histories, we examined divergence of OP shape from that of the anadromous ancestor. We report preliminary evidence for divergence between benthic and generalist lake ecotypes, necessitating further investigation. Furthermore, rapid divergence of OP shape has occurred in a lake population that was founded by anadromous stickleback in the 1980s, which is consistent with divergence of other phenotypic traits and with OP diversification in other lake populations. By contrast, there has been limited evolution of OP shape in a second lake population that may have experienced a genetic bottleneck early in its history and lacks genetic variation for OP divergence. Taken together, the results obtained from these two populations are consistent with studies of other stickleback phenotypic traits that implicate ancestral variation in postglacial adaptive radiation of threespine stickleback in fresh water.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 832–844.     

Parallels,nonparallels, and plasticity in population differentiation of threespine stickleback within a lake

The frequent occurrence of parallel phenotypic divergence in similar habitats is often evoked when emphasizing the role of ecology in adaptive radiation and speciation. However, because phenotypic plasticity can contribute to the observed pattern of divergence, confirmation of divergence at loci underlying phenotypic traits is important for confirming adaptive divergence. In the present study, we examine parallel morphological, neutral, and potentially adaptive genetic divergence of threespine stickleback inhabiting different habitats within a lake. Three genetic clusters best explained the neutral genetic structure within the lake; however, morphological differences were only weakly connected to genetic clusters and there was considerable phenotypic variation within clusters. Among the factors that could contribute to the observed pattern of morphological and genetic divergence are phenotypic plasticity, selective mortality of hybrids, and habitat choice based on morphology. Several loci are identified as outliers indicating divergent selection between the morphs and some parallels in morphological and adaptive genetic divergence are found in stickleback spawning at two lava sites. However, neutral genetic structure indicates considerable genetic connectivity among the two lava sites, and the parallels in morphology may therefore represent selective distribution of phenotypes rather than parallel divergence. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 803–813.     

Genomic variation at the tips of the adaptive radiation of Darwin's finches

Adaptive radiation unfolds as selection acts on the genetic variation underlying functional traits. The nature of this variation can be revealed by studying the tips of an ongoing adaptive radiation. We studied genomic variation at the tips of the Darwin's finch radiation; specifically focusing on polymorphism within, and variation among, three sympatric species of the genus Geospiza. Using restriction site‐associated DNA (RAD‐seq), we characterized 32 569 single‐nucleotide polymorphisms (SNPs), from which 11 outlier SNPs for beak and body size were uncovered by a genomewide association study (GWAS). Principal component analysis revealed that these 11 SNPs formed four statistically linked groups. Stepwise regression then revealed that the first PC score, which included 6 of the 11 top SNPs, explained over 80% of the variation in beak size, suggesting that selection on these traits influences multiple correlated loci. The two SNPs most strongly associated with beak size were near genes associated with beak morphology across deeper branches of the radiation: delta‐like 1 homologue (DLK1) and high‐mobility group AT‐hook 2 (HMGA2). Our results suggest that (i) key adaptive traits are associated with a small fraction of the genome (11 of 32 569 SNPs), (ii) SNPs linked to the candidate genes are dispersed throughout the genome (on several chromosomes), and (iii) micro‐ and macro‐evolutionary variation (roots and tips of the radiation) involve some shared and some unique genomic regions.     

HOW MUCH OF THE VARIATION IN ADAPTIVE DIVERGENCE CAN BE EXPLAINED BY GENE FLOW? AN EVALUATION USING LAKE‐STREAM STICKLEBACK PAIRS

Abstract How much of the variation in adaptive divergence can be explained by gene flow? The answer to this question should objectively reveal whether gene flow generally places a substantial constraint on evolutionary diversification. We studied multiple independent lake‐stream population pairs of threespine stickleback (Gasterosteus acu‐leatus). For each pair, we quantified adaptive divergence based on morphological traits that have a genetic basis and are subject to divergent selection. We then estimated gene flow based on variation at five unlinked microsatellite loci. We found a consistent and significant pattern for morphological divergence to be positively correlated with genetic divergence and negatively correlated with gene flow. Statistical significance and the amount of variation explained varied within and among traits: 36.1–74.1% for body depth and 11.8–51.7% for gill raker number. Variation within each trait was the result of differences among methods for estimating genetic divergence and gene flow. Variation among traits likely reflects different strengths of divergent selection. We conclude that gene flow has a substantial effect on adaptive divergence in nature but that the magnitude of this effect varies among traits. An alternative explanation is that cause and effect are reversed: adaptive divergence is instead constraining gene flow. This effect seems relatively unimportant for our system because genetic divergence and gene flow were not correlated with ecologically relevant habitat features of lakes (surface area) or streams (width, depth, flow, canopy openness).