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.
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
. 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
. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs
, 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
. 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.
Abstract
Homoploid hybrid speciation (i.e., hybrid speciation without a change in ploidy) has traditionally been considered to be rare in animals. Only few accepted empirical examples of homoploid ...hybrid speciation in nature exist, and in only one previous case (insects) was it convincingly shown that this process occurred in complete sympatry. Here, we report an instance of sympatric homoploid hybrid speciation in Midas cichlid fishes in Crater Lake Xiloá, Nicaragua. The hybrid lineage, albeit at an early stage of speciation, has genomically and phenotypically diverged from both of its two parental species. Together with a distinct stable isotope signature this suggests that this hybrid lineages occupies a different trophic niche compared to the other sympatric Midas cichlid species in Crater Lake Xiloá.
The identification of thousands of variants across the genomes and their accurate genotyping are crucial for estimating the genetic parameters needed to address a host of molecular ecological and ...evolutionary questions. With rapid advances of massively parallel high‐throughput sequencing technologies, several methods have recently been developed to access genomewide data on population variation. One of the most successful and widely used techniques relies on the combination of restriction enzymes and sequencing‐by‐synthesis: restriction‐site‐associated DNA sequencing (RADSeq). We developed a new, more time‐ and cost‐efficient double‐digest RAD paired‐end protocol (quaddRAD) that simplifies and speeds up the identification of PCR duplicates and permits large‐scale multiplexing. Assessing its performance on a technical data set, we also applied the quaddRAD method on population samples of a Neotropical cichlid fish lineage (Archocentrus centrarchus) to assess its genetic structure and demographic history. While we identified allopatric interlake genetic divergence, most likely driven by drift, no signature of sympatric divergence was detected. This differs from what has been observed in the clade of Midas cichlids (Amphilophus citrinellus spp.), another cichlid lineage that inhabits the same lakes and shares a similar demographic history, but has evolved into small‐scale adaptive radiations via sympatric speciation. We demonstrate that quaddRAD is a robust and efficient method for genotyping a massive number and widely overlapping set of loci with high accuracy. Furthermore, the results on A. centrarchus open new research avenues providing an ideal system to investigate genome‐level mechanisms that could alter the speciation potential of different but closely related cichlid lineages.
Abstract
Chromosomal evolution is widely considered to be an important driver of speciation, as karyotypic reorganization can bring about the establishment of reproductive barriers between incipient ...species. One textbook example for genetic mechanisms of speciation are large-scale chromosomal rearrangements such as Robertsonian (Rb) fusions, a common class of structural variants that can drastically change the recombination landscape by suppressing crossing-over and influence gene expression by altering regulatory networks. Here, we explore the population structure and demographic patterns of a well-known house mouse Rb system in the Aeolian archipelago in Southern Italy using genome-wide data. By analyzing chromosomal regions characterized by different levels of recombination, we trace the evolutionary history of a set of Rb chromosomes occurring in different geographical locations and test whether chromosomal fusions have a single shared origin or occurred multiple times. Using a combination of phylogenetic and population genetic approaches, we find support for multiple, independent origins of three focal Rb chromosomes. The elucidation of the demographic patterns of the mouse populations within the Aeolian archipelago shows that an interplay between fixation of newly formed Rb chromosomes and hybridization events has contributed to shaping their current karyotypic distribution. Overall, our results illustrate that chromosome structure is much more dynamic than anticipated and emphasize the importance of large-scale chromosomal translocations in speciation.
Fundamental to understanding how biodiversity arises and adapts is whether evolution is predictable in the face of stochastic genetic and demographic factors. Here we show rapid parallel evolution ...across two closely related but geographically isolated radiations of Nicaraguan crater lake cichlid fishes. We find significant morphological, ecological and genetic differentiation between ecomorphs in sympatry, reflected primarily in elongated versus high-bodied shape, differential ecological niche use and genetic differentiation. These eco-morphological divergences are significantly parallel across radiations. Based on 442,644 genome-wide single nucleotide polymorphisms, we identify strong support for the monophyly of, and subsequent sympatric divergence within, each radiation. However, the order of speciation differs across radiations; in one lake the limnetic ecomorph diverged first while in the other a benthic ecomorph. Overall our results demonstrate that complex parallel phenotypes can evolve very rapidly and repeatedly in similar environments, probably due to natural selection, yet this evolution can proceed along different evolutionary genetic routes.
After a volcano erupts, a lake may form in the cooled crater and become an isolated aquatic ecosystem. This makes fishes in crater lakes informative for understanding sympatric evolution and ...ecological diversification in barren environments. From a geological and limnological perspective, such research offers insight about the process of crater lake ecosystem establishment and speciation. In the present study we use genetic and coalescence approaches to infer the colonization history of Midas cichlid fishes (Amphilophus cf. citrinellus) that inhabit a very young crater lake in Nicaragua-the ca. 1800 year-old Lake Apoyeque. This lake holds two sympatric, endemic morphs of Midas cichlid: one with large, hypertrophied lips (approximately 20% of the total population) and another with thin lips. Here we test the associated ecological, morphological and genetic diversification of these two morphs and their potential to represent incipient speciation.
Gene coalescence analyses 11 microsatellite loci and mitochondrial DNA (mtDNA) sequences suggest that crater lake Apoyeque was colonized in a single event from the large neighbouring great lake Managua only about 100 years ago. This founding in historic times is also reflected in the extremely low nuclear and mitochondrial genetic diversity in Apoyeque. We found that sympatric adult thin- and thick-lipped fishes occupy distinct ecological trophic niches. Diet, body shape, head width, pharyngeal jaw size and shape and stable isotope values all differ significantly between the two lip-morphs. The eco-morphological features pharyngeal jaw shape, body shape, stomach contents and stable isotopes (delta15N) all show a bimodal distribution of traits, which is compatible with the expectations of an initial stage of ecological speciation under disruptive selection. Genetic differentiation between the thin- and thick-lipped population is weak at mtDNA sequence (FST = 0.018) and absent at nuclear microsatellite loci (FST < 0.001).
This study provides empirical evidence of eco-morphological differentiation occurring very quickly after the colonization of a new and vacant habitat. Exceptionally low levels of neutral genetic diversity and inference from coalescence indicates that the Midas cichlid population in Apoyeque is much younger (ca. 100 years or generations old) than the crater itself (ca. 1 800 years old). This suggests either that the crater remained empty for many hundreds of years after its formation or that remnant volcanic activity prevented the establishment of a stable fish population during the early life of the crater lake. Based on our findings of eco-morphological variation in the Apoyeque Midas cichlids, and known patterns of adaptation in Midas cichlids in general, we suggest that this population may be in a very early stage of speciation (incipient species), promoted by disruptive selection and ecological diversification.
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.
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.
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 Amphilophus 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 probably resulted in morphological and physiological trade‐offs that contributed to the rapid establishment and maintenance of divergence with gene flow.
see also the Perspective by Gaither et al
PDF
