scholarly journals The cryptic origins of evolutionary novelty: 1,000-fold-faster trophic diversification rates without increased ecological opportunity or hybrid swarm

2016 ◽  
Author(s):  
Christopher H. Martin
Keyword(s):  
Gene Flow ◽  
Adaptive Radiation ◽  
Fitness Landscape ◽  
Morphological Diversity ◽  
Hybrid Swarm ◽  
Ecological Opportunity ◽  
San Salvador ◽  
San Salvador Island ◽  
Or Gene ◽  
Trophic Diversification

AbstractEcological opportunity is frequently proposed as the sole ingredient for adaptive radiation into novel niches. Alternatively, genome-wide hybridization resulting from ‘hybrid swarm’ may be the trigger. However, these hypotheses have been difficult to test due to the rarity of comparable control environments lacking adaptive radiations. Here I exploit such a pattern in microendemic radiations of Caribbean pupfishes. I show that a sympatric three-species radiation on San Salvador Island, Bahamas diversified 1,445 times faster than neighboring islands in jaw length due to evolution of a novel scale-eating adaptive zone from a generalist ancestral niche. I then sampled 22 generalist populations on seven neighboring islands and measured morphological diversity, stomach content diversity, dietary isotopic diversity, genetic diversity, lake/island areas, macroalgae richness, and Caribbean-wide patterns of gene flow. None of these standard metrics of ecological opportunity or gene flow were associated with adaptive radiation, except for slight increases in macroalgae richness. Thus, exceptional trophic diversification is highly localized despite myriad generalist populations in comparable environmental and genetic backgrounds. This study provides a strong counterexample to the ecological/hybrid-swarm theories of adaptive radiation and suggests that diversification of novel specialists on a sparse fitness landscape is constrained by more than ecological opportunity and gene flow.

scholarly journals A vertebrate adaptive radiation is assembled from an ancient and disjunct spatiotemporal landscape

2021 ◽  
Vol 118 (20) ◽  
pp. e2011811118
Author(s):  
Emilie J. Richards ◽  
Joseph A. McGirr ◽  
Jeremy R. Wang ◽  
Michelle E. St. John ◽  
Jelmer W. Poelstra ◽  
...  
Keyword(s):  
Adaptive Radiation ◽  
Population Genomics ◽  
De Novo ◽  
Nonsynonymous Substitution ◽  
Adaptive Divergence ◽  
Hybrid Swarm ◽  
Regulatory Variation ◽  
San Salvador ◽  
Standing Variation ◽  
San Salvador Island

To investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of adaptive alleles underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. On a single Bahamian island, ancient standing variation from disjunct geographic sources was reassembled into new combinations under strong directional selection for adaptation to the novel trophic niches of scale-eating and molluscivory. We found evidence for two longstanding hypotheses of adaptive radiation: hybrid swarm origins and temporal stages of adaptation. Using a combination of population genomics, transcriptomics, and genome-wide association mapping, we demonstrate that this microendemic adaptive radiation of novel trophic specialists on San Salvador Island, Bahamas experienced twice as much adaptive introgression as generalist populations on neighboring islands and that adaptive divergence occurred in stages. First, standing regulatory variation in genes associated with feeding behavior (prlh, cfap20, and rmi1) were swept to fixation by selection, then standing regulatory variation in genes associated with craniofacial and muscular development (itga5, ext1, cyp26b1, and galr2) and finally the only de novo nonsynonymous substitution in an osteogenic transcription factor and oncogene (twist1) swept to fixation most recently. Our results demonstrate how ancient alleles maintained in distinct environmental refugia can be assembled into new adaptive combinations and provide a framework for reconstructing the spatiotemporal landscape of adaptation and speciation.

scholarly journals Evolution of the locomotor skeleton in Anolis lizards reflects the interplay between ecological opportunity and phylogenetic inertia

2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Nathalie Feiner ◽  
Illiam S. C. Jackson ◽  
Edward L. Stanley ◽  
Tobias Uller
Keyword(s):  
Adaptive Radiation ◽  
Morphological Diversity ◽  
Evolutionary Rates ◽  
Greater Antilles ◽  
Ecological Opportunity ◽  
Morphological Diversification ◽  
Phylogenetic Inertia ◽  
Evolutionary Trajectories ◽  
Repeated Evolution ◽  
Variable Evolutionary Rates

AbstractAnolis lizards originated in continental America but have colonized the Greater Antillean islands and recolonized the mainland, resulting in three major groups (Primary and Secondary Mainland and Greater Antillean). The adaptive radiation in the Greater Antilles has famously resulted in the repeated evolution of ecomorphs. Yet, it remains poorly understood to what extent this island radiation differs from diversification on the mainland. Here, we demonstrate that the evolutionary modularity between girdles and limbs is fundamentally different in the Greater Antillean and Primary Mainland Anolis. This is consistent with ecological opportunities on islands driving the adaptive radiation along distinct evolutionary trajectories. However, Greater Antillean Anolis share evolutionary modularity with the group that recolonized the mainland, demonstrating a persistent phylogenetic inertia. A comparison of these two groups support an increased morphological diversity and faster and more variable evolutionary rates on islands. These macroevolutionary trends of the locomotor skeleton in Anolis illustrate that ecological opportunities on islands can have lasting effects on morphological diversification.

scholarly journals Don’t throw out the sympatric species with the crater lake water: fine-scale investigation of introgression provides weak support for functional role of secondary gene flow in one of the clearest examples of sympatric speciation

2017 ◽  
Author(s):  
Emilie J. Richards ◽  
Jelmer W. Poelstra ◽  
Christopher H. Martin
Keyword(s):  
Gene Flow ◽  
Crater Lake ◽  
Morphological Diversity ◽  
Sympatric Speciation ◽  
Sympatric Species ◽  
Fine Scale ◽  
Ancestral Polymorphism ◽  
Hybrid Swarm ◽  
Weak Support ◽  
History Of

AbstractGenomic data has revealed complex histories of colonization and repeated gene flow previously unrecognized in some of the most celebrated examples of sympatric speciation and radiation. However, much of the evidence for secondary gene flow into these radiations comes from genome-wide tests, which tells us little about how gene flow potentially influenced sympatric diversification. Here we investigated whole genomes of Barombi Mbo crater lake cichlids for fine-scale patterns of introgression between species with neighboring riverine cichlid populations. We did find evidence of secondary gene flow into the radiation scattered across < 0.24% of the genome; however, the functional and genetic diversity in these regions paint no clear picture of how that variation could have contributed to the ecological and morphological diversity found in the lake. Our results suggest that either variation in novel genetic pathways introduced during secondary gene flow contributed to the radiation, or that secondary gene flow was predominantly neutral with respect to the diversification processes. We also found evidence for differential assortment of ancestral polymorphism found in riverine populations between sympatric sister species, suggesting the presence of a hybrid swarm in the past. While the history of gene flow and colonization appears to be more complicated than once thought, the lack of compelling evidence for secondary gene flow influencing diversification suggests that we should not yet rule out one of the most celebrated examples of sympatric speciation in nature.

scholarly journals The coincidence of ecological opportunity with hybridization explains rapid adaptive radiation in Lake Mweru cichlid fishes

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Joana I. Meier ◽  
Rike B. Stelkens ◽  
Domino A. Joyce ◽  
Salome Mwaiko ◽  
Numel Phiri ◽  
...  
Keyword(s):  
Genetic Variation ◽  
Gene Flow ◽  
Great Lakes ◽  
Adaptive Radiation ◽  
Ecological Opportunity ◽  
African Great Lakes ◽  
Cichlid Fishes ◽  
Haplochromine Cichlid ◽  
Genetic Potential ◽  
Adaptive Radiations

AbstractThe process of adaptive radiation was classically hypothesized to require isolation of a lineage from its source (no gene flow) and from related species (no competition). Alternatively, hybridization between species may generate genetic variation that facilitates adaptive radiation. Here we study haplochromine cichlid assemblages in two African Great Lakes to test these hypotheses. Greater biotic isolation (fewer lineages) predicts fewer constraints by competition and hence more ecological opportunity in Lake Bangweulu, whereas opportunity for hybridization predicts increased genetic potential in Lake Mweru. In Lake Bangweulu, we find no evidence for hybridization but also no adaptive radiation. We show that the Bangweulu lineages also colonized Lake Mweru, where they hybridized with Congolese lineages and then underwent multiple adaptive radiations that are strikingly complementary in ecology and morphology. Our data suggest that the presence of several related lineages does not necessarily prevent adaptive radiation, although it constrains the trajectories of morphological diversification. It might instead facilitate adaptive radiation when hybridization generates genetic variation, without which radiation may start much later, progress more slowly or never occur.

scholarly journals Adaptive introgression and de novo mutations increase access to novel fitness peaks on the fitness landscape during a vertebrate adaptive radiation

2021 ◽  
Author(s):  
Austin H. Patton ◽  
Emilie Richards ◽  
Katelyn J. Gould ◽  
Logan K. Buie ◽  
Christopher Herbert Martin
Keyword(s):  
Genetic Variation ◽  
Adaptive Radiation ◽  
De Novo ◽  
Fitness Landscape ◽  
Adaptive Landscape ◽  
Ecological Niches ◽  
San Salvador ◽  
Adaptive Introgression ◽  
Independent Field ◽  
Adaptive Walks

Estimating the complex relationship between fitness and genotype or phenotype (i.e. the adaptive landscape) is one of the central goals of evolutionary biology. Empirical fitness landscapes have now been estimated for numerous systems, from phage to proteins to finches. However, the nature of adaptive walks connecting genotypes to organismal fitness, speciation, and novel ecological niches are still poorly understood. One outstanding system for addressing these connections is a recent adaptive radiation of ecologically and morphologically distinct pupfishes (a generalist, molluscivore, and scale-eater) endemic to San Salvador Island, Bahamas. Here, we leveraged whole-genome sequencing of 139 hybrids from two independent field fitness experiments to identify the genomic basis of fitness, visualize the first genotypic fitness networks in a vertebrate system, and infer the contributions of different sources of genetic variation to the accessibility of the fitness landscape. We identified 132 SNPs that were significantly associated with fitness in field enclosures, including six associated genes that were differentially expressed between specialists, and one gene (protein-lysine methyltransferase: METTL21E) misexpressed in hybrids, suggesting a potential intrinsic genetic incompatibility. We then constructed genotypic fitness networks from adaptive alleles and show that only introgressed and de novo variants, not standing genetic variation, increased the accessibility of genotypic fitness paths from generalist to specialists. Our results suggest that adaptive introgression and de novo variants provided key connections in adaptive walks necessary for crossing fitness valleys and triggering the evolution of novelty during adaptive radiation.

scholarly journals Field manipulation of competition among hybrids reveals dynamic and highly stable features of a complex fitness landscape driving adaptive radiation

2019 ◽  
Author(s):  
Christopher H. Martin ◽  
Katelyn Gould
Keyword(s):  
Adaptive Radiation ◽  
Prey Capture ◽  
Fitness Landscape ◽  
Fitness Landscapes ◽  
Competitive Environment ◽  
Adaptive Landscape ◽  
Dynamic Features ◽  
Environmental Variance ◽  
San Salvador ◽  
Independent Field

AbstractThe effect of the environment on fitness in natural populations is a fundamental question in evolutionary biology. However, experimental manipulations of environment and phenotype are rare. Thus, the relative importance of the competitive environment versus intrinsic organismal performance in shaping the location, height, and fluidity of fitness peaks and valleys remains largely unknown. We experimentally tested the effect of competitive environment on the fitness landscape driving the evolution of novelty in a sympatric adaptive radiation of a generalist and two trophic specialist pupfishes, a scale-eater and molluscivore, endemic to San Salvador Island, Bahamas. We manipulated phenotypes, by generating 2,611 F4/F5 lab-reared hybrids, and competitive environment, by altering frequencies of rare phenotypes between high- and low-frequency field enclosures, then tracked hybrid survival in two natural lake populations on San Salvador. We found no evidence of frequency-dependent effects on survival fitness landscapes, indicating robustness to the competitive environment. Although survival surfaces favored alternate phenotypes between lakes, joint fitness estimation across lake environments supported multiple fitness peaks for generalist and molluscivore phenotypes and a large fitness valley isolating the most divergent scale-eater phenotype, strikingly similar to a previous independent field experiment. The consistency of this complex fitness landscape across competitive environments, multivariate trait axes, and spatiotemporal heterogeneity provides surprising evidence of stasis in major features of fitness landscapes despite substantial environmental variance, possibly due to absolute biomechanical constraints on diverse prey capture strategies within this radiation. These results challenge competitive speciation theory and highlight the interplay between organism and environment underlying static and dynamic features of the adaptive landscape.

scholarly journals How to Investigate the Origins of Novelty: Insights Gained from Genetic, Behavioral, and Fitness Perspectives

2019 ◽  
Vol 1 (1) ◽  
Author(s):  
C H Martin ◽  
J A McGirr ◽  
E J Richards ◽  
M E St. John
Keyword(s):  
Fitness Landscape ◽  
Natural World ◽  
Adaptive Divergence ◽  
Ecological Niches ◽  
San Salvador ◽  
Novel Traits ◽  
San Salvador Island ◽  
Rapid Radiations ◽  
Evolutionary Novelties

Synopsis Biologists are drawn to the most extraordinary adaptations in the natural world, often referred to as evolutionary novelties, yet rarely do we understand the microevolutionary context underlying the origins of novel traits, behaviors, or ecological niches. Here we discuss insights gained into the origins of novelty from a research program spanning biological levels of organization from genotype to fitness in Caribbean pupfishes. We focus on a case study of the origins of novel trophic specialists on San Salvador Island, Bahamas and place this radiation in the context of other rapid radiations. We highlight questions that can be addressed about the origins of novelty at different biological levels, such as measuring the isolation of novel phenotypes on the fitness landscape, locating the spatial and temporal origins of adaptive variation contributing to novelty, detecting dysfunctional gene regulation due to adaptive divergence, and connecting behaviors with novel traits. Evolutionary novelties are rare, almost by definition, and we conclude that integrative case studies can provide insights into this rarity relative to the dynamics of adaptation to more common ecological niches and repeated parallel speciation, such as the relative isolation of novel phenotypes on fitness landscapes and the transient availability of ecological, genetic, and behavioral opportunities.

scholarly journals Continental cichlid radiations: functional diversity reveals the role of changing ecological opportunity in the Neotropics

2016 ◽  
Vol 283 (1836) ◽  
pp. 20160556 ◽  
Author(s):  
Jessica Hilary Arbour ◽  
Hernán López-Fernández
Keyword(s):  
Central America ◽  
Adaptive Radiation ◽  
Morphological Diversity ◽  
Evolutionary Rates ◽  
Ecological Niches ◽  
Ecological Opportunity ◽  
Ecological Release ◽  
Adaptive Radiations ◽  
Lineage Diversification

Adaptive radiations have been hypothesized to contribute broadly to the diversity of organisms. Models of adaptive radiation predict that ecological opportunity and ecological release, the availability of empty ecological niches and the response by adapting lineages to occupy them, respectively, drive patterns of phenotypic and lineage diversification. Adaptive radiations driven by ‘ecological opportunity’ are well established in island systems; it is less clear if ecological opportunity influences continent-wide diversification. We use Neotropical cichlid fishes to test if variation in rates of functional evolution is consistent with changing ecological opportunity. Across a functional morphological axis associated with ram–suction feeding traits, evolutionary rates declined through time as lineages diversified in South America. Evolutionary rates of ram–suction functional morphology also appear to have accelerated as cichlids colonized Central America and encountered renewed opportunity. Our results suggest that ecological opportunity may play an important role in shaping patterns of morphological diversity of even broadly distributed lineages like Neotropical cichlids.

scholarly journals Adaptive introgression from distant Caribbean islands contributed to the diversification of a microendemic radiation of trophic specialist pupfishes

2017 ◽  
Author(s):  
Emilie J. Richards ◽  
Christopher H. Martin
Keyword(s):  
Genetic Variation ◽  
Adaptive Radiation ◽  
Evolutionary Relationships ◽  
Selective Sweeps ◽  
Multiple Sources ◽  
San Salvador ◽  
Adaptive Introgression ◽  
Evolutionary Relatedness ◽  
San Salvador Island ◽  
Specialist Species

AbstractRapid diversification often involves complex histories of gene flow that leave variable and conflicting signatures of evolutionary relatedness across the genome. Identifying the extent and source of variation in these evolutionary relationships can provide insight into the evolutionary mechanisms involved in rapid radiations. Here we compare the discordant evolutionary relationships associated with species phenotypes across 42 whole genomes from a sympatric adaptive radiation of Cyprinodon pupfishes endemic to San Salvador Island, Bahamas and several outgroup pupfish species in order to understand the rarity of these trophic specialists within the larger radiation of Cyprinodon. 82% of the genome depicts close evolutionary relationships among the San Salvador Island species reflecting their geographic proximity, but the vast majority of the fixed variants between the specialist species lie in regions with discordant topologies. These regions include signatures of selective sweeps and adaptive introgression from neighboring islands into each of the specialist species. Hard selective sweeps of genetic variation on San Salvador contributed 10-fold more to divergence between specialist species within the radiation than adaptive introgression of Caribbean genetic variation; however, some of these introgressed regions from distant islands were associated with the primary axis of oral jaw divergence within the radiation. For example, standing variation in a proto-oncogene (ski) known to have effects on jaw size introgressed into one San Salvador specialist from an island 300 km away. The complex emerging picture of the origins of adaptive radiation on San Salvador indicates that multiple sources of genetic variation contributed to the adaptive phenotypes of novel trophic specialists on the island. Our findings suggest that a suite of factors, including rare adaptive introgression, may also be required to trigger adaptive radiation in the presence of ecological opportunity.Author summaryGroups of closely related species can rapidly evolve to occupy diverse ecological roles, but the ecological and genetic conditions that trigger this diversification are still highly debated. We examine patterns of molecular evolution across the genomes of a rapid radiation of pupfishes that includes two trophic specialists. Despite apparently widespread ecological opportunities and gene flow across the Caribbean, this radiation is endemic to a single Bahamian Island. Using the whole genomes of 42 pupfish we find evidence of extensive and previously unexpected variation in evolutionary relatedness among Caribbean pupfish. Two sources of genetic variation have contributed to the adaptive diversification of complex phenotypes in this system: selective sweeps of genetic variation from across the Caribbean that was brought into San Salvador through hybridization and genetic variation found on San Salvador. While genetic variation from San Salvador appears to be relatively more common in the divergence observed among specialists, hybridization probably played an important role in the evolution of the complex phenotypes as well. Our findings that multiple sources of genetic variation contribute to the San Salvador radiation suggest that a complex suite of factors, including hybridization with other species, may be required to trigger adaptive radiation in the presence of ecological opportunity.

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