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

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.

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

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2016.0556 ◽

2016 ◽

Vol 283 (1836) ◽

pp. 20160556 ◽

Cited By ~ 15

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.

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Conservation and Convergence of Genetic Architecture in the Adaptive Radiation ofAnolislizards

10.1101/2021.02.18.431064 ◽

2021 ◽

Author(s):

Joel W. McGlothlin ◽

Megan E. Kobiela ◽

Helen V. Wright ◽

Jason J. Kolbe ◽

Jonathan B. Losos ◽

...

Keyword(s):

Adaptive Radiation ◽

Genetic Architecture ◽

Recurrent Selection ◽

Phylogenetic Signal ◽

Genetic Correlations ◽

Greater Antilles ◽

Evolutionary Constraint ◽

Response To Selection ◽

Repeated Evolution ◽

Habitat Specialists

ABSTRACTTheGmatrix, which quantifies the genetic architecture of traits, is often viewed as an evolutionary constraint. However,Gcan evolve in response to selection and may also be viewed as a product of adaptive evolution. The evolution of similarGmatrices in similar environments would suggest thatGevolves adaptively, but it is difficult to disentangle such effects from phylogeny. Here, we use the adaptive radiation ofAnolislizards to ask whether convergence ofGaccompanies the repeated evolution of habitat specialists, or ecomorphs, across the Greater Antilles. We measuredGin seven species representing three ecomorphs (trunk-crown, trunk-ground, and grass-bush). We found that the overall structure ofGdoes not converge. Instead, the structure ofGis well conserved and displays a phylogenetic signal. However, several elements ofGshowed signatures of convergence, indicating that some aspects of genetic architecture have been shaped by selection. Most notably, genetic correlations between limb traits and body traits were weaker in long-legged trunk-ground species, suggesting effects of recurrent selection on limb length. Our results demonstrate that common selection pressures may have subtle but consistent effects on the evolution ofG, even as the overall pattern of genetic architecture remains conserved.

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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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Faculty Opinions recommendation of Ecological opportunity in adaptive radiation of Galápagos endemic land snails.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1281969.748072 ◽

2009 ◽

Author(s):

Jonathan Shurin ◽

Travis Ingram

Keyword(s):

Adaptive Radiation ◽

Land Snails ◽

Ecological Opportunity

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Variation in pleiotropic hub gene expression is associated with interspecific differences in head shape and eye size in Drosophila

Molecular Biology and Evolution ◽

10.1093/molbev/msaa335 ◽

2021 ◽

Author(s):

Elisa Buchberger ◽

Anıl Bilen ◽

Sanem Ayaz ◽

David Salamanca ◽

Cristina Matas de las Heras ◽

...

Keyword(s):

Natural Variation ◽

Compound Eye ◽

Genetic Manipulation ◽

Morphological Evolution ◽

Morphological Diversity ◽

Network Evolution ◽

Head Shape ◽

Eye Size ◽

Recurrent Mutations ◽

Repeated Evolution

Abstract Revealing the mechanisms underlying the breath-taking morphological diversity observed in nature is a major challenge in Biology. It has been established that recurrent mutations in hotspot genes cause the repeated evolution of morphological traits, such as body pigmentation or the gain and loss of structures. To date, however, it remains elusive whether hotspot genes contribute to natural variation in the size and shape of organs. Since natural variation in head morphology is pervasive in Drosophila, we studied the molecular and developmental basis of differences in compound eye size and head shape in two closely related Drosophila species. We show differences in the progression of retinal differentiation between species and we applied comparative transcriptomics and chromatin accessibility data to identify the GATA transcription factor Pannier (Pnr) as central factor associated with these differences. Although the genetic manipulation of Pnr affected multiple aspects of dorsal head development, the effect of natural variation is restricted to a subset of the phenotypic space. We present data suggesting that this developmental constraint is caused by the co-evolution of expression of pnr and its co-factor u-shaped (ush). We propose that natural variation in expression or function of highly connected developmental regulators with pleiotropic functions is a major driver for morphological evolution and we discuss implications on gene regulatory network evolution. In comparison to previous findings, our data strongly suggests that evolutionary hotspots are not the only contributors to the repeated evolution of eye size and head shape in Drosophila.

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Intraspecific adaptive radiation: Competition, ecological opportunity, and phenotypic diversification within species

Evolution ◽

10.1111/evo.13313 ◽

2017 ◽

Vol 71 (10) ◽

pp. 2496-2509 ◽

Cited By ~ 9

Author(s):

Nicholas A. Levis ◽

Ryan A. Martin ◽

Kerry A. O'Donnell ◽

David W. Pfennig

Keyword(s):

Adaptive Radiation ◽

Ecological Opportunity ◽

Phenotypic Diversification

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Patterns of morphological diversification in giant Berberomeloe blister beetles (Coleoptera: Meloidae) reveal an unexpected taxonomic diversity concordant with mtDNA phylogenetic structure

Zoological Journal of the Linnean Society ◽

10.1093/zoolinnean/zlz164 ◽

2020 ◽

Vol 189 (4) ◽

pp. 1249-1312 ◽

Cited By ~ 1

Author(s):

Alberto Sánchez-Vialas ◽

Mario García-París ◽

José L Ruiz ◽

Ernesto Recuero

Keyword(s):

New Species ◽

Genetic Variability ◽

Phenotypic Variability ◽

Morphological Diversity ◽

Taxonomic Diversity ◽

Molecular Data ◽

Species Boundaries ◽

Congeneric Species ◽

Phylogenetic Structure ◽

Morphological Diversification

Abstract Delimiting species boundaries is a complex challenge usually hindered by overlooked morphological diversification or misinterpretation of geographically structured phenotypic variability. Independent molecular data are extremely useful to characterize and understand such morphological diversity. Morphological and molecular variability of the non-phoretic and apterous, widely distributed, giant blister beetles of the genus Berberomeloe, were investigated within and between lineages across most of the distributional range of the genus. We used two mtDNA gene fragments to characterize genetic variability and to produce a time-calibrated phylogeny of the genus. Our results reveal several mitochondrial lineages, allopatrically, parapatrically and sympatrically distributed. Most clades are not distinguishable between each other based on morphometrics. However, no morphometric overlap is observed between two closely related clades, one of them occurring in sympatry with a distantly congeneric species (B. insignis), suggesting that sympatry could trigger morphological diversification. Although most species share a morphometric space, they can be morphologically identified by a combination of easily observed characteristic qualitative features. Based on the concordance between mtDNA clades and morphological units, we describe six new species of Berberomeloe (B. castuo sp. nov., B. comunero sp. nov., B. indalo sp. nov, B. yebli sp. nov., B. payoyo sp. nov. and B. tenebrosus sp. nov.), revalidate two taxa (B. maculifrons comb. nov. and B. laevigatus comb. nov.) and redefine B. majalis.

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HOW DOES ECOLOGICAL OPPORTUNITY INFLUENCE RATES OF SPECIATION, EXTINCTION, AND MORPHOLOGICAL DIVERSIFICATION IN NEW WORLD RATSNAKES (TRIBE LAMPROPELTINI)?

Evolution ◽

10.1111/j.1558-5646.2009.00888.x ◽

2009 ◽

Vol 64 (4) ◽

pp. 934-943 ◽

Cited By ~ 72

Author(s):

Frank T. Burbrink ◽

R. Alexander Pyron

Keyword(s):

New World ◽

Ecological Opportunity ◽

Morphological Diversification

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Radiation of tropical island bees and the role of phylogenetic niche conservatism as an important driver of biodiversity

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2020.0045 ◽

2020 ◽

Vol 287 (1925) ◽

pp. 20200045

Author(s):

James B. Dorey ◽

Scott V. C. Groom ◽

Elisha H. Freedman ◽

Cale S. Matthews ◽

Olivia K. Davies ◽

...

Keyword(s):

Adaptive Radiation ◽

Morphological Data ◽

Niche Conservatism ◽

Single Nucleotide ◽

Tropical Island ◽

Phylogenetic Niche Conservatism ◽

Phylogenetic Inertia ◽

Island Biodiversity ◽

Future Warming

Island biogeography explores how biodiversity in island ecosystems arises and is maintained. The topographical complexity of islands can drive speciation by providing a diversity of niches that promote adaptive radiation and speciation. However, recent studies have argued that phylogenetic niche conservatism, combined with topographical complexity and climate change, could also promote speciation if populations are episodically fragmented into climate refugia that enable allopatric speciation. Adaptive radiation and phylogenetic niche conservatism therefore both predict that topographical complexity should encourage speciation, but they differ strongly in their inferred mechanisms. Using genetic (mitochondrial DNA (mtDNA) and single-nucleotide polymorphism (SNP)) and morphological data, we show high species diversity (22 species) in an endemic clade of Fijian Homalictus bees, with most species restricted to highlands and frequently exhibiting narrow geographical ranges. Our results indicate that elevational niches have been conserved across most speciation events, contradicting expectations from an adaptive radiation model but concordant with phylogenetic niche conservatism. Climate cycles, topographical complexity, and niche conservatism could interact to shape island biodiversity. We argue that phylogenetic niche conservatism is an important driver of tropical island bee biodiversity but that this phylogenetic inertia also leads to major extinction risks for tropical ectotherms under future warming climates.

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