Contrasting signatures of genomic divergence during sympatric speciation.

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 Darwin1,2. 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 process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, 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 histories5. 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.

Implementing Large Genomic Single Nucleotide Polymorphism Data Sets in Phylogenetic Network Reconstructions: A Case Study of Particularly Rapid Radiations of Cichlid Fish.

The Midas cichlids of the Amphilophus citrinellus spp. species complex from Nicaragua (13 species) are an extraordinary example of adaptive and rapid radiation ($<$24,000 years old). These cichlids are a very challenging group to infer its evolutionary history in phylogenetic analyses, due to the apparent prevalence of incomplete lineage sorting (ILS), as well as past and current gene flow. Assuming solely a vertical transfer of genetic material from an ancestral lineage to new lineages is not appropriate in many cases of genes transferred horizontally in nature. Recently developed methods to infer phylogenetic networks under such circumstances might be able to circumvent these problems. These models accommodate not just ILS, but also gene flow, under the multispecies network coalescent (MSNC) model, processes that are at work in young, hybridizing, and/or rapidly diversifying lineages. There are currently only a few programs available that implement MSNC for estimating phylogenetic networks. Here, we present a novel way to incorporate single nucleotide polymorphism (SNP) data into the currently available PhyloNetworks program. Based on simulations, we demonstrate that SNPs can provide enough power to recover the true phylogenetic network. We also show that it can accurately infer the true network more often than other similar SNP-based programs (PhyloNet and HyDe). Moreover, our approach results in a faster algorithm compared to the original pipeline in PhyloNetworks, without losing power. We also applied our new approach to infer the phylogenetic network of Midas cichlid radiation. We implemented the most comprehensive genomic data set to date (RADseq data set of 679 individuals and $>$37K SNPs from 19 ingroup lineages) and present estimated phylogenetic networks for this extremely young and fast-evolving radiation of cichlid fish. We demonstrate that the MSNC is more appropriate than the multispecies coalescent alone for the analysis of this rapid radiation. [Genomics; multispecies network coalescent; phylogenetic networks; phylogenomics; RADseq; SNPs.].

Phylogenomic data resolve higher-level relationships within South American Liolaemus lizards.

Phylogenomic approaches now generate hundreds of loci representative of the whole genome that can be used for phylogenetic analyses. The South American lizard genus Liolaemus is the most species-rich vertebrate radiation from temperate zones (more than 265 described species), yet most higher-level phylogenetic relationships within Liolaemus remain poorly resolved. In this study, we used 584 nuclear loci collected using targeted sequenced capture to estimate the phylogenetic relationships among 26 species representing the two subgenera within Liolaemus (Eulaemus + Liolaemus), and all major groups within Eulaemus. Previous molecular and morphological-based phylogenetic analyses of Eulaemus based on a limited number of characters resolved few higher-level relationships, although one point of agreement is that the early divergence within Eulaemus corresponds to the lineomaculatus section, followed by the diversification of eight main clades that are strongly supported and recognized. Liolaemus probably experienced relatively rapid divergences during parts of its evolutionary history, and a phylogenomic approach was used to resolve the relationships among the major groups. The new analyses presented here support the division of Liolaemus into two subgenera, and resolve relationships among many of the major clades of Eulaemus with strong support. A Bayesian divergence dating analysis using 44 protein-coding genes provides an estimation of the split of the two Liolaemus subgenera of approximately 19,7 ma (95% HPD = 16,94-23,04), while diversification within Eulaemus started at 15,05 ma (95% HPD = 12,94 - 17,59) among the L. lineomaculatus and the L. montanus series by Mid Miocene. A novel phylogenetic network analyses for SNP data identified two hybridizing edges among different groups of Eulaemus at different points in time. Having a solid phylogenetic hypothesis of the main Eulaemus clades opens new opportunities to test a variety of macroevolutionary questions for this unique radiation.

Phylogenomics of a putatively convergent novelty: did hypertrophied lips evolve once or repeatedly in Lake Malawi cichlid fishes?

BACKGROUND: Phylogenies provide critical information about convergence during adaptive radiation. To test whether there have been multiple origins of a distinctive trophic phenotype in one of the most rapidly radiating groups known, we used ultra-conserved elements (UCEs) to examine the evolutionary affinities of Lake Malawi cichlids lineages exhibiting greatly hypertrophied lips. RESULTS: The hypertrophied lip cichlids Cheilochromis euchilus, Eclectochromis ornatus, Placidochromis "Mbenji fatlip", and Placidochromis milomo are all nested within the non-mbuna clade of Malawi cichlids based on both concatenated sequence and single nucleotide polymorphism (SNP) inferred phylogenies. Lichnochromis acuticeps that exhibits slightly hypertrophied lips also appears to have evolutionary affinities to this group. However, Chilotilapia rhoadesii that lacks hypertrophied lips was recovered as nested within the species Cheilochromis euchilus. Species tree reconstructions and analyses of introgression provided largely ambiguous patterns of Malawi cichlid evolution. CONCLUSIONS: Contrary to mitochondrial DNA phylogenies, bifurcating trees based on our 1024 UCE loci supported close affinities of Lake Malawi lineages with hypertrophied lips. However, incomplete lineage sorting in Malawi tends to render these inferences more tenuous. Phylogenomic analyses will continue to provide powerful inferences about whether phenotypic novelties arose once or multiple times during adaptive radiation.

Evidence of body size and shape stasis driven by selection in Patagonian lizards of the Phymaturus patagonicus clade (Squamata: Liolaemini).

During the speciation process sibling lineages accumulate differences in time (e.g. genetic, morphological, and/or ecological). Phenotypic traits such as size or shape, however, could experience rapid changes or show stasis depending on their role in survival and reproduction. The clade Phymaturus patagonicus includes 26 species characterized by a conservative morphology, and all inhabit rock crevice microhabitats in arid environments. In this study we quantify levels of morphological divergence (size and shape) among the multiple species relative to interspecific molecular divergence, and show that most species have not diverged significantly in size and/or shape to permit unambiguous species diagnosis with morphological data alone. The influence of stabilizing selection for an adaptive optimum in body size and head shape was detected for 13 of the 16 variables analyzed in an Ornstein-Uhlenbeck model. The strict dependence of these species to rock-crevice microenvironments likely explains the observed morphological stasis across the many species of the Phymaturus patagonicus group.

Hybridization could be a common phenomenon within the highly diverse lizard genus Liolaemus.

Hybridization is likely to occur more often between closely related taxa that have had insufficient time to diverge to the point of reproductive incompatibility; hybridization between deeply divergent lineages is rare. In squamate reptiles, hybridization has been proposed as a possible explanation for the extensive paraphyly observed in mitochondrial gene trees in several species complexes of the South American lizard genus Liolaemus. One of the best-documented cases is within the L. boulengeri and L. rothi complexes, which diverged ~5.5 million years ago. Here, we describe a comprehensive study for approaching the hybridization hypothesis between these lizard species complexes. We explored the level of gene tree discordance using the novel 'extra lineage contribution' statistics (XLC, presented in this study) that quantifies the level of gene tree discordance contribution per individual within a species. We included molecular data (12 nuclear and two mitochondrial genes) from 127 individuals, and results of a coalescent model-based analysis show that the most likely explanation for the gene tree-species tree discordance is interspecific hybridization. Our best-supported hypothesis suggests current and past hybridization between L. rothi (rothi complex) and L. tehuelche (boulengeri complex), and independently between L. rothi and L. boulengeri and L. telsen (boulengeri complex). The hybrid descendants are characterized by intermediate phenotypes between the parental species, but are more similar to L. rothi in body size. We discuss the possible role of hybridization in Liolaemus evolution.

Hidden diversity within the lizard genus Liolaemus: Genetic vs morphological divergence in the L. rothi complex (Squamata:Liolaeminae).

Currently, Liolaemus is the second most species-rich reptile genus in the world (257 species), and predictions of its real diversity suggest that it may be the most diverse genus. Originally, Liolaemus species were described as widely distributed and morphologically variable taxa, but extensive sampling in previously unexplored geographic areas, coupled with molecular and more extensive morphological studies, have discovered an unexpectedly high number of previously undetected species. Here, we study the level of molecular vs. morphological divergence within the L. rothi complex, combining a total of 14 loci (2 mitochondrial and 12 nuclear loci) for 97 individuals, as well as morphological data (nine morphometric and 15 color pattern variables), that represent all six described species of the L. rothi complex, plus two candidate species. We use the multi-coalescent species delimitation program iBPP and resolve strong differences in molecular divergence; and each species is inferred as an independent lineage supported by high posterior probabilities. However, morphological differences are not that clear, and our modeling of morphological characters suggests differential selection pressures implying some level of morphological stasis. We discuss the role of natural selection on phenotypic traits, which may be an important factor in "hiding" the real diversity of the genus.

Digest: Liolaemus lizards as an emerging model system to study hybridization as a driver of rapid radiations.

Recent perspectives on speciation genomics emphasize the pivotal role of hybridization in driving rapid radiations. The Liolaemus lizard genus displays impressive species richness with around 290 species widely distributed across southern South America. Sánchez et al. conducted a comprehensive study on the 5-million-year-old Liolaemus kingii group, which includes 14 species. The research provides new key insights to enhance our understanding of this rapid radiation, including its diversification in space and time and the consequences of hybridization in its morphological evolution and taxonomy.

The South American genus Cnemalobus (Coleoptera: Carabidae: Cnemalobini): phylogeny and biogeographic analysis with the description of four new species from extra-Andean Patagonian mountains.

The carabid beetle Cnemalobus Guérin-Ménéville, 1838 inhabits high- and lowland grasslands of southern South America. The highest diversity is found in the Patagonian Steppe, where distribution patterns are associated with latitude and elevation. Northern Patagonia, a large volcanic region with a complex geoclimatic history, exhibits elevated grades of endemism. However, a great deal remains unknown regarding diversification and biogeographical patterns for most of the endemic groups. We describe new Cnemalobus species restricted to isolated volcanoes from these extra-Andean mountain systems. We assess the phylogenetic relationships by updating the phylogeny of the genus and conduct a Bayesian binary Markov chain-Monte Carlo (MCMC) analysis on the resulting phylogenetic tree to discuss the biogeographical distribution patterns. We also provide a taxonomic key to all currently known species of Cnemalobus from the Patagonian Steppe. Our phylogenetic analysis supports the monophyly of the new species Cnemalobus tromen sp. nov., Cnemalobus silviae sp. nov., Cnemalobus aucamahuida sp. nov. and Cnemalobus domuyo sp. nov. grouped with C. diamante and C. nevado , referred to as the 'Extra-Andean' mountain lineage. Biogeographical analysis recognises vicariant events as the most plausible explanation for the allopatric distributions of the new species. We hypothesise that these vicariant events could be related to climatic barriers that likely promoted speciation processes by generating geographical isolation in ancestral populations. Our findings contribute significantly to the biogeographical understanding of the Patagonian volcanic region, prompting new inquiries to unravel the speciation processes of the endemic biota in extra-Andean mountain systems. ZooBank: urn:lsid:zoobank.org:pub:6A7585E8-5006-45BC-A1A3-F874F18A6049.

Molecular phylogenetic relationships of the Liolaemus rothi complex and a new species of lizard from Auca Mahuida Volcano (Squamata: Liolaemini).

A new species of lizard of the genus Liolaemus from Neuquén Province, western Argentina, is described. The new species is a member of the Liolaemus rothi species complex, and mitochondrial and nuclear molecular data show it as sister taxon of the clade composed of (L. hermannunezi (L. tromen + L. loboi)), differing in size, squamation, coloration, and sexual dimorphism from the other species of this group. Liolaemus sitesi sp. nov. has a dark body coloration with series of notched blotches on the dorsum, with bright spots, and a very iridescent yellow-green coloration in natural light. Liolaemus sitesi sp. nov. is found only in the Auca Mahuida volcano and is terrestrial, dwelling on the stony slopes with sandy soil between 1300 m and the volcano summit.

Early stages of sympatric homoploid hybrid speciation in crater lake cichlid fishes.

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.

Evidence of hybridization in the Argentinean lizards Liolaemus gracilis and Liolaemus bibronii (IGUANIA: LIOLAEMINI): an integrative approach based on genes and morphology.

The lizard genus Liolaemus is endemic to temperate South America and includes more than 225 species. Liolaemus gracilis and L. bibronii are closely related species that have large and overlapping geographic distributions, and the objective of this work is to further investigate the L. bibronii-L. gracilis mtDNA paraphyletic pattern previously detected, using an integrative approach, based on mtDNA, nuclear DNA and morphological characters. We identified eight morphological L. bibronii introgressed with L. gracilis mtDNAs, and the reciprocal for one L. gracilis, from six localities in the region of sympatry overlap. The morphological identity of these introgressed individuals was confirmed by diagnostic nuclear markers, and this represents the first well-documented case of interspecific hybridization in the lizard genus Liolaemus. Of the three most likely hypotheses for these observed patterns, we suggest that asymmetrical mtDNA introgression as a result of recent or ongoing hybridization between L. bibronii and L. gracilis is the most likely. This may be due to size selection by L. gracilis female preference for the larger L. bibroni males in sympatry, but this requires experimental confirmation.

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.