Genomic signatures of admixture and selection are shared among populations of <i>Zaprionus indianus</i> across the western hemisphere

Introduced species have become an increasingly common component of biological communities around the world. A central goal in invasion biology is therefore to identify the demographic and evolutionary factors that underlie successful introductions. Here we use whole genome sequences, collected from populations in the native and introduced range of the African fig fly, Zaprionus indianus, to quantify genetic relationships among them, identify potential sources of the introductions, and test for selection at different spatial scales. We find that geographically widespread populations in the western hemisphere are genetically more similar to each other than to lineages sampled across Africa, and that these populations share a mixture of alleles derived from differentiated African lineages. Using patterns of allele‐sharing and demographic modelling we show that Z. indinaus have undergone a single expansion across the western hemisphere with admixture between African lineages predating this expansion. We also find support for selection that is shared across populations in the western hemisphere, and in some cases, with a subset of African populations. This suggests either that parallel selection has acted across a large part of Z. indianus's introduced range; or, more parsimoniously, that Z. indianus has experienced selection early on during (or prior‐to) its expansion into the western hemisphere. We suggest that the range expansion of Z. indianus has been facilitated by admixture and selection, and that management of this invasion could focus on minimizing future admixture by controlling the movement of individuals within this region rather than between the western and eastern hemisphere

Lessons from a natural experiment: Allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way

Explaining why some lineages diversify while others do not and how are key objectives in evolutionary biology. Young radiations of closely related species derived from the same source population provide an excellent opportunity to disentangle the relative contributions of possible drivers of diversification. In these settings, lineage‐specific effects are shared and can be ruled out. Moreover, the relevant demographic and ecological parameters can be estimated accurately. Midas cichlid fish in Nicaragua have repeatedly colonized several crater lakes, diverged from the same source populations, and, interestingly, diversified in some of them but not others. Here, using the most comprehensive molecular and geometric morphometric data set on Midas cichlids to date (∼20,000 SNPs, 12 landmarks, ∼700 individuals), we aim to understand why and how crater lake populations diverge and why some of them are more prone to diversify in sympatry than others. Taking ancestor‐descendant relationships into account, we find that Midas cichlids diverged in parallel from their source population mostly—but not exclusively—by evolving more slender body shapes in all six investigated crater lakes. Admixture among crater lakes has possibly facilitated this process in one case, but overall, admixture and secondary waves of colonization cannot predict morphological divergence and intralacustrine diversification. Instead, morphological divergence is larger the more dissimilar a crater lake is compared to the source lake and happens rapidly after colonization followed by a slow‐down with time. Our data also provide some evidence that founder effects may positively contribute to divergence. The depth of a crater lake is positively associated with variation in body shapes (and number of species), presumably by providing more ecological opportunities. In conclusion, we find that parallel morphological divergence in allopatry and the propensity for diversification in sympatry across the entire Midas cichlid fish radiation is partly predictable and mostly driven by ecology.publishe

An intronic transposon insertion associates with a trans-species color polymorphism in Midas cichlid fishes

Polymorphisms have fascinated biologists for a long time, but their genetic underpinnings often remain elusive. Here, we aim to uncover the genetic basis of the gold/dark polymorphism that is eponymous of Midas cichlid fish (Amphilophus spp.) adaptive radiations in Nicaraguan crater lakes. While most Midas cichlids are of the melanic “dark morph”, about 10% of individuals lose their melanic pigmentation during their ontogeny and transition into a conspicuous “gold morph”. Using a new haplotype-resolved long-read assembly we discover an 8.2 kb, transposon-derived inverted repeat in an intron of an undescribed gene, which we term goldentouch in reference to the Greek myth of King Midas. The gene goldentouch is differentially expressed between morphs, presumably due to structural implications of inverted repeats in both DNA and/or RNA (cruciform and hairpin formation). The near-perfect association of the insertion with the phenotype across independent populations suggests that it likely underlies this trans-specific, stable polymorphism.Peer reviewe

Diving into divergence: Differentiation in swimming performances, physiology and gene expression between locally‐adapted sympatric cichlid fishes

Sympatric speciation occurs without geographical barriers and is thought to often be driven by ecological specialization of individuals that eventually diverge genetically and phenotypically. Distinct morphologies between sympatric populations occupying different niches have been interpreted as such differentiating adaptive phenotypes, yet differences in performance and thus likely adaptiveness between them were rarely tested. Here, we investigated if divergent body shapes of two sympatric crater lake cichlid species from Nicaragua, one being a shore‐associated (benthic) species while the other prefers the open water zones (limnetic), affect cruising (Ucrit) and sprinting (Usprint) swimming abilities ‐ performances particularly relevant to their respective lifestyles. Furthermore, we investigated species differences in oxygen consumption (MO2) across different swimming speeds and compare gene expression in gills and white muscle at rest and during exercise. We found a superior cruising ability in the limnetic Amphilophus zaliosus compared to the benthic A. astorquii, while sprinting was not different, suggesting that their distinct morphologies affect swimming performance. Increased cruising swimming ability in A. zaliosus was linked to a higher oxygen demand during activity (but not rest), indicating different metabolic rates during exercise ‐ a hypothesis supported by coinciding gene expression patterns of gill transcriptomes. We identified differentially expressed genes linked to swimming physiology, regulation of swimming behaviour and oxygen intake. A combination of physiological and morphological differences may thus underlie adaptations to these species’ distinct niches. This complex ecological specialization likely resulted in morphological and physiological trade‐offs that contributed to the rapid establishment and maintenance of divergence with gene flow

Contrasting signatures of genomic divergence during sympatric speciation

Population genomic analyses of Midas cichlid fishes in young Nicaraguan crater lakes suggest that sympatric speciation is promoted by polygenic architectures. The transition from 'well-marked varieties' of a single species into 'well-defined species'-especially in the absence of geographic barriers to gene flow (sympatric speciation)-has puzzled evolutionary biologists ever since Darwin(1,2). Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process(3). Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs(4), but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories(5). Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry.Peer reviewe

Evolution of gene expression across brain regions in behaviourally divergent deer mice.

peer reviewedThe evolution of innate behaviours is ultimately due to genetic variation likely acting in the nervous system. Gene regulation may be particularly important because it can evolve in a modular brain-region specific fashion through the concerted action of cis- and trans-regulatory changes. Here, to investigate transcriptional variation and its regulatory basis across the brain, we perform RNA sequencing (RNA-Seq) on ten brain subregions in two sister species of deer mice (Peromyscus maniculatus and P. polionotus)-which differ in a range of innate behaviours, including their social system-and their F1 hybrids. We find that most of the variation in gene expression distinguishes subregions, followed by species. Interspecific differential expression (DE) is pervasive (52-59% of expressed genes), whereas the number of DE genes between sexes is modest overall (~3%). Interestingly, the identity of DE genes varies considerably across brain regions. Much of this modularity is due to cis-regulatory divergence, and while 43% of genes were consistently assigned to the same gene regulatory class across subregions (e.g. conserved, cis- or trans-regulatory divergence), a similar number were assigned to two or more different gene regulatory classes. Together, these results highlight the modularity of gene expression differences and divergence in the brain, which may be key to explain how the evolution of brain gene expression can contribute to the astonishing diversity of animal behaviours

Genome sequences reveal global dispersal routes and suggest convergent genetic adaptations in seahorse evolution

Seahorses have a circum-global distribution in tropical to temperate coastal waters. Yet, seahorses show many adaptations for a sedentary, cryptic lifestyle: they require specific habitats, such as seagrass, kelp or coral reefs, lack pelvic and caudal fins, and give birth to directly developed offspring without pronounced pelagic larval stage, rendering long-range dispersal by conventional means inefficient. Here we investigate seahorses’ worldwide dispersal and biogeographic patterns based on a de novo genome assembly of Hippocampus erectus as well as 358 re-sequenced genomes from 21 species. Seahorses evolved in the late Oligocene and subsequent circum-global colonization routes are identified and linked to changing dynamics in ocean currents and paleo-temporal seaway openings. Furthermore, the genetic basis of the recurring “bony spines” adaptive phenotype is linked to independent substitutions in a key developmental gene. Analyses thus suggest that rafting via ocean currents compensates for poor dispersal and rapid adaptation facilitates colonizing new habitats.Fil: Chunyan, Li. Southern Marine Science and Engineering Guangdong Laboratory; China. Pilot National Laboratory for Marine Science and Technology; China. Chinese Academy of Sciences; República de ChinaFil: Olave, Melisa. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Provincia de Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Universidad Nacional de Cuyo. Instituto Argentino de Investigaciones de las Zonas Áridas; Argentina. University of Konstanz; AlemaniaFil: Hou, Yali. Chinese Academy of Sciences; República de ChinaFil: Geng, Qi. Chinese Academy of Sciences; República de China. Southern Marine Science and Engineering Guangdong Laboratory; ChinaFil: Schneider, Ralf. University Of Konstanz; Alemania. Helmholtz Centre for Ocean Research Kie; AlemaniaFil: Zeixa, Gao. Huazhong Agricultural University; ChinaFil: Xiaolong, Tu. Allwegene Technologies ; ChinaFil: Xin, Wang. Chinese Academy of Sciences; República de ChinaFil: Furong, Qi. China National Center for Bioinformation; China. University of Chinese Academy of Sciences; ChinaFil: Nater, Alexander. University of Konstanz; AlemaniaFil: Kautt, Andreas F.. University of Konstanz; Alemania. Harvard University; Estados UnidosFil: Wan, Shiming. Chinese Academy of Sciences; República de ChinaFil: Yanhong, Zhang. Chinese Academy of Sciences; República de ChinaFil: Yali, Liu. Chinese Academy of Sciences; República de ChinaFil: Huixian, Zhang. Chinese Academy of Sciences; República de ChinaFil: Bo, Zhang. Chinese Academy of Sciences; República de ChinaFil: Hao, Zhang. Chinese Academy of Sciences; República de ChinaFil: Meng, Qu ,. Chinese Academy of Sciences; República de ChinaFil: Shuaishuai, Liu. Chinese Academy of Sciences; República de ChinaFil: Zeyu, Chen. Chinese Academy of Sciences; República de China. University of Chinese Academy of Sciences; ChinaFil: Zhong, Jia. Chinese Academy of Sciences; República de ChinaFil: Zhang, He. BGI-Shenzhen; ChinaFil: Meng, Lingfeng. BGI-Shenzhen; ChinaFil: Wang, Kai. Ludong University; ChinaFil: Yin, Jianping. Chinese Academy of Sciences; República de ChinaFil: Huang, Liangmin. Chinese Academy of Sciences; República de China. University of Chinese Academy of Sciences; ChinaFil: Venkatesh, Byrappa. Institute of Molecular and Cell Biology; SingapurFil: Meyer, Axel. University of Konstanz; AlemaniaFil: Lu, Xuemei. Chinese Academy of Sciences; República de ChinaFil: Lin, Qiang. Chinese Academy of Sciences; República de China. Southern Marine Science and Engineering Guangdong Laboratory; China. Pilot National Laboratory for Marine Science and Technology; China. University of Chinese Academy of Sciences; Chin

Genome-wide Patterns of Adaptation and Speciation and Demographic Histories of Young Radiations of Cichlids

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Multispecies Outcomes of Sympatric Speciation after Admixture with the Source Population in Two Radiations of Nicaraguan Crater Lake Cichlids

The formation of species in the absence of geographic barriers (i.e. sympatric speciation) remains one of the most controversial topics in evolutionary biology. While theoretical models have shown that this most extreme case of primary divergence-with-gene-flow is possible, only a handful of accepted empirical examples exist. And even for the most convincing examples uncertainties remain; complex histories of isolation and secondary contact can make species falsely appear to have originated by sympatric speciation. This alternative scenario is notoriously difficult to rule out. Midas cichlids inhabiting small and remote crater lakes in Nicaragua are traditionally considered to be one of the best examples of sympatric speciation and lend themselves to test the different evolutionary scenarios that could lead to apparent sympatric speciation since the system is relatively small and the source populations known. Here we reconstruct the evolutionary history of two small-scale radiations of Midas cichlids inhabiting crater lakes Apoyo and Xiloá through a comprehensive genomic data set. We find no signs of differential admixture of any of the sympatric species in the respective radiations. Together with coalescent simulations of different demographic models our results support a scenario of speciation that was initiated in sympatry and does not result from secondary contact of already partly diverged populations. Furthermore, several species seem to have diverged simultaneously, making Midas cichlids an empirical example of multispecies outcomes of sympatric speciation. Importantly, however, the demographic models strongly support an admixture event from the source population into both crater lakes shortly before the onset of the radiations within the lakes. This opens the possibility that the formation of reproductive barriers involved in sympatric speciation was facilitated by genetic variants that evolved in a period of isolation between the initial founding population and the secondary migrants that came from the same source population. Thus, the exact mechanisms by which these species arose might be different from what had been thought before.publishe

Syndrome des loges du membre inférieur

Divergent selection is the main driving force in sympatric ecological speciation and may also play a strong role in divergence between allopatric populations. Characterizing the genome-wide impact of divergent selection constitutes often a first step in the process of unraveling the genetic bases underlying adaptation and ecological speciation. The Midas cichlid fish (Amphilophus citrinellus) species complex in Nicaragua is a powerful system for studying evolutionary processes. Independent colonizations of isolated young crater lakes by Midas cichlid populations from the older and great lakes of Nicaragua resulted in the repeated evolution of adaptive radiations by intralacustrine sympatric speciation. In this study we performed genome scans on two repeated radiations of crater lake species and their great lake source populations (1030 polymorphic AFLPs, n ≈ 30 individuals per species). We detected regions under divergent selection (0.3 % in the crater lake Xiloá flock and 1.7 % in the older crater lake Apoyo radiation) that might be responsible for the sympatric diversification. We find no evidence that the same genomic regions have been involved across crater lake flocks. The data provide evidence, however, for some genetic parallelism (seven out of 51 crater lake to great lake outlier loci are shared; 13.7%) associated with the allopatric divergence of both crater lake flocks. Furthermore, our results suggest that the number of outlier loci involved in sympatric and allopatric divergence increases with time. A phylogeny based on our data clearly supports the monophyly of both crater lake species flocks and provides evidence for a parallel branching order with a primary divergence along the limnetic-benthic axis in both radiations