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Successive climate crises in the deep past drove the early evolution and radiation of reptiles.

ABSTRACT: Climate change-induced mass extinctions provide unique opportunities to explore the impacts of global environmental disturbances on organismal evolution. However, their influence on terrestrial ecosystems remains poorly understood. Here, we provide a new time tree for the early evolution of reptiles and their closest relatives to reconstruct how the Permian-Triassic climatic crises shaped their long-term evolutionary trajectory. By combining rates of phenotypic evolution, mode of selection, body size, and global temperature data, we reveal an intimate association between reptile evolutionary dynamics and climate change in the deep past. We show that the origin and phenotypic radiation of reptiles was not solely driven by ecological opportunity following the end-Permian extinction as previously thought but also the result of multiple adaptive responses to climatic shifts spanning 57 million years.

SUBMITTER: Simoes TR

PROVIDER: S-EPMC9390993 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Successive climate crises in the deep past drove the early evolution and radiation of reptiles.

Simões Tiago R TR Kammerer Christian F CF Caldwell Michael W MW Pierce Stephanie E SE

Science advances 20220819 33

Climate change-induced mass extinctions provide unique opportunities to explore the impacts of global environmental disturbances on organismal evolution. However, their influence on terrestrial ecosystems remains poorly understood. Here, we provide a new time tree for the early evolution of reptiles and their closest relatives to reconstruct how the Permian-Triassic climatic crises shaped their long-term evolutionary trajectory. By combining rates of phenotypic evolution, mode of selection, body ...[more]

PMID: 35984885

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Project description:Background and aimsADP-glucose pyrophosphorylase (AGPase) is a key enzyme of starch biosynthesis. In the green plant lineage, it is composed of two large (LSU) and two small (SSU) sub-units encoded by paralogous genes, as a consequence of several rounds of duplication. First, our aim was to detect specific patterns of molecular evolution following duplication events and the divergence between monocotyledons and dicotyledons. Secondly, we investigated coevolution between amino acids both within and between sub-units.MethodsA phylogeny of each AGPase sub-unit was built using all gymnosperm and angiosperm sequences available in databases. Accelerated evolution along specific branches was tested using the ratio of the non-synonymous to the synonymous substitution rate. Coevolution between amino acids was investigated taking into account compensatory changes between co-substitutions.Key resultsWe showed that SSU paralogues evolved under high functional constraints during angiosperm radiation, with a significant level of coevolution between amino acids that participate in SSU major functions. In contrast, in the LSU paralogues, we identified residues under positive selection (1) following the first LSU duplication that gave rise to two paralogues mainly expressed in angiosperm source and sink tissues, respectively; and (2) following the emergence of grass-specific paralogues expressed in the endosperm. Finally, we found coevolution between residues that belong to the interaction domains of both sub-units.ConclusionsOur results support the view that coevolution among amino acid residues, especially those lying in the interaction domain of each sub-unit, played an important role in AGPase evolution. First, within SSU, coevolution allowed compensating mutations in a highly constrained context. Secondly, the LSU paralogues probably acquired tissue-specific expression and regulatory properties via the coevolution between sub-unit interacting domains. Finally, the pattern we observed during LSU evolution is consistent with repeated sub-functionalization under 'Escape from Adaptive Conflict', a model rarely illustrated in the literature.

Project description:BackgroundSimpson envisaged a conceptual model of adaptive radiation in which lineages diversify into "adaptive zones" within a macroevolutionary adaptive landscape. However, only a handful of studies have empirically investigated this adaptive landscape and its consequences for our interpretation of the underlying mechanisms of phenotypic evolution. In fish radiations the evolution of locomotor phenotypes may represent an important dimension of ecomorphological diversification given the implications of locomotion for feeding and habitat use. Neotropical geophagine cichlids represent a newly identified adaptive radiation and provide a useful system for studying patterns of locomotor diversification and the implications of selective constraints on phenotypic divergence in general.ResultsWe use multivariate ordination, models of phenotypic evolution and posterior predictive approaches to investigate the macroevolutionary adaptive landscape and test for evidence of early divergence of locomotor phenotypes in Geophagini. The evolution of locomotor phenotypes was characterized by selection towards at least two distinct adaptive peaks and the early divergence of modern morphological disparity. One adaptive peak included the benthic and epibenthic invertivores and was characterized by fishes with deep, laterally compressed bodies that optimize precise, slow-swimming manoeuvres. The second adaptive peak resulted from a shift in adaptive optima in the species-rich ram-feeding/rheophilic Crenicichla-Teleocichla clade and was characterized by species with streamlined bodies that optimize fast starts and rapid manoeuvres. Evolutionary models and posterior predictive approaches favoured an early shift to a new adaptive peak over decreasing rates of evolution as the underlying process driving the early divergence of locomotor phenotypes.ConclusionsThe influence of multiple adaptive peaks on the divergence of locomotor phenotypes in Geophagini is compatible with the expectations of an ecologically driven adaptive radiation. This study confirms that the diversification of locomotor phenotypes represents an important dimension of phenotypic evolution in the geophagine adaptive radiation. It also suggests that the commonly observed early burst of phenotypic evolution during adaptive radiations may be better explained by the concentration of shifts to new adaptive peaks deep in the phylogeny rather than overall decreasing rates of evolution.

Dataset Information

Successive climate crises in the deep past drove the early evolution and radiation of reptiles.

Publications

Successive climate crises in the deep past drove the early evolution and radiation of reptiles.

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