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

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.

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

10.1101/053140 ◽

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.

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Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato

10.1101/000208 ◽

2013 ◽

Author(s):

Nicola Nadeau ◽

Mayte Ruiz ◽

Patricio Salazar ◽

Brian Counterman ◽

Jose Alejandro Medina ◽

...

Keyword(s):

Population Genomics ◽

De Novo ◽

Reference Sequence ◽

Colour Pattern ◽

Adaptive Divergence ◽

Population Divergence ◽

Hybrid Zones ◽

Data Alignment ◽

Parallel Hybrid ◽

Genomic Regions

Hybrid zones can be valuable tools for studying evolution and identifying genomic regions responsible for adaptive divergence and underlying phenotypic variation. Hybrid zones between subspecies of Heliconius butterflies can be very narrow and are maintained by strong selection acting on colour pattern. The co-mimetic species H. erato and H. melpomene have parallel hybrid zones where both species undergo a change from one colour pattern form to another. We use restriction associated DNA sequencing to obtain several thousand genome wide sequence markers and use these to analyse patterns of population divergence across two pairs of parallel hybrid zones in Peru and Ecuador. We compare two approaches for analysis of this type of data; alignment to a reference genome and de novo assembly, and find that alignment gives the best results for species both closely (H. melpomene) and distantly (H. erato, ~15% divergent) related to the reference sequence. Our results confirm that the colour pattern controlling loci account for the majority of divergent regions across the genome, but we also detect other divergent regions apparently unlinked to colour pattern differences. We also use association mapping to identify previously unmapped colour pattern loci, in particular the Ro locus. Finally, we identify within our sample a new cryptic population of H. timareta in Ecuador, which occurs at relatively low altitude and is mimetic with H. melpomene malleti.

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Major stages of vertebrate adaptive radiation are assembled from a disparate spatiotemporal landscape

10.1101/2020.03.12.988774 ◽

2020 ◽

Cited By ~ 2

Author(s):

Emilie J. Richards ◽

Joseph A. McGirr ◽

Jeremy R. Wang ◽

Michelle E. St. John ◽

Jelmer W. Poelstra ◽

...

Keyword(s):

Adaptive Radiation ◽

Genetic Variants ◽

De Novo ◽

Craniofacial Development ◽

Standing Variation ◽

Three Stages ◽

The Caribbean ◽

Selection For ◽

Trophic Niches ◽

Clear Support

AbstractTo investigate the origins and stages of vertebrate adaptive radiation, we reconstructed the spatial and temporal histories of genetic variants underlying major phenotypic axes of diversification from the genomes of 202 Caribbean pupfishes. Ancient standing variation from disparate spatial sources was reassembled into new combinations which are under strong selection for adaptation to novel trophic niches on only a single island throughout the Caribbean. This occurred in three stages: first, standing variation associated with feeding behavior swept, then standing variation regulating craniofacial development and pigmentation, and finally de novo variation for craniofacial development. Our results provide clear support for two longstanding hypotheses about adaptive radiation and demonstrate how ancient alleles maintained for millennia in distinct environmental refugia can be assembled into new adaptive combinations.One Sentence SummaryAncient origins of adaptive radiation

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Introgressive hybridization facilitates adaptive divergence in a recent radiation of monkeyflowers

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.1666 ◽

2015 ◽

Vol 282 (1814) ◽

pp. 20151666 ◽

Cited By ~ 53

Author(s):

Sean Stankowski ◽

Matthew A. Streisfeld

Keyword(s):

Evolutionary Biology ◽

De Novo ◽

Phylogenetic Analyses ◽

Introgressive Hybridization ◽

Flower Colour ◽

Adaptive Divergence ◽

Evolutionary Mechanisms ◽

Standing Variation ◽

Regulatory Mutations ◽

History Of

A primary goal in evolutionary biology is to identify the historical events that have facilitated the origin and spread of adaptations. When these adaptations also lead to reproductive isolation, we can learn about the evolutionary mechanisms contributing to speciation. We reveal the complex history of the gene MaMyb2 in shaping flower colour divergence within a recent radiation of monkeyflowers. In the Mimulus aurantiacus species complex, red-flowered M. a. ssp . puniceus and yellow-flowered M. a. ssp. australis are partially isolated because of differences in pollinator preferences. Phylogenetic analyses based on genome-wide variation across the complex suggest two origins of red flowers from a yellow-flowered ancestor: one in M. a. ssp . puniceus and one in M. a. ssp. flemingii . However, in both cases, red flowers are caused by cis -regulatory mutations in the gene MaMyb2 . Although this could be due to distinct mutations in each lineage, we show that the red allele in M. a. ssp. puniceus did not evolve de novo or exist as standing variation in its yellow-flowered ancestor. Rather, our results suggest that a single red MaMyb2 allele evolved during the radiation of M. aurantiacus that was subsequently transferred to the yellow-flowered ancestor of M. a. ssp. puniceus via introgressive hybridization. Because gene flow is still possible among taxa, we conclude that introgressive hybridization can be a potent driver of adaptation at the early stages of divergence that can contribute to the origins of biodiversity.

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

10.1101/2021.07.01.450666 ◽

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.

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

Integrative Organismal Biology ◽

10.1093/iob/obz018 ◽

2019 ◽

Vol 1 (1) ◽

Cited By ~ 3

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.

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

10.1101/115055 ◽

2017 ◽

Cited By ~ 5

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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