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Parallel evolution of genes controlling mitonuclear balance in short-lived annual fishes.

ABSTRACT: The current molecular understanding of the aging process derives almost exclusively from the study of random or targeted single-gene mutations in highly inbred laboratory species, mostly invertebrates. Little information is available as to the genetic mechanisms responsible for natural lifespan variation and the evolution of lifespan, especially in vertebrates. Here, we investigated the pattern of positive selection in annual (i.e., short-lived) and nonannual (i.e., longer-lived) African killifishes to identify a genomic substrate for evolution of annual life history (and reduced lifespan). We identified genes under positive selection in all steps of mitochondrial biogenesis: mitochondrial (mt) DNA replication, transcription from mt promoters, processing and stabilization of mt RNAs, mt translation, assembly of respiratory chain complexes, and electron transport chain. Signs of paralleled evolution (i.e., evolution in more than one branch of Nothobranchius phylogeny) are observed in four out of five steps. Moreover, some genes under positive selection in Nothobranchius are under positive selection also in long-lived mammals such as bats and mole-rats. Complexes of the respiratory chain are formed in a coordinates multistep process where nuclearly and mitochondrially encoded components are assembled and inserted into the inner mitochondrial membrane. The coordination of this process is named mitonuclear balance, and experimental manipulations of mitonuclear balance can increase longevity of laboratory species. Our data strongly indicate that these genes are also casually linked to evolution lifespan in vertebrates.

SUBMITTER: Sahm A

PROVIDER: S-EPMC5418189 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Parallel evolution of genes controlling mitonuclear balance in short-lived annual fishes.

Sahm Arne A Bens Martin M Platzer Matthias M Cellerino Alessandro A

Aging cell 20170311 3

The current molecular understanding of the aging process derives almost exclusively from the study of random or targeted single-gene mutations in highly inbred laboratory species, mostly invertebrates. Little information is available as to the genetic mechanisms responsible for natural lifespan variation and the evolution of lifespan, especially in vertebrates. Here, we investigated the pattern of positive selection in annual (i.e., short-lived) and nonannual (i.e., longer-lived) African killifi ...[more]

PMID: 28295945

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Project description:BackgroundEarly evolutionary theories of aging predict that populations which experience low extrinsic mortality evolve a retarded onset of senescence. Experimental support for this theory in vertebrates is scarce, in part for the difficulty of quantifying extrinsic mortality and its condition- and density-dependent components that -when considered- can lead to predictions markedly different to those of the "classical" theories. Here, we study annual fish of the genus Nothobranchius whose maximum lifespan is dictated by the duration of the water bodies they inhabit. Different populations of annual fish do not experience different strengths of extrinsic mortality throughout their life span, but are subject to differential timing (and predictability) of a sudden habitat cessation. In this respect, our study allows testing how aging evolves in natural environments when populations vary in the prospect of survival, but condition-dependent survival has a limited effect. We use 10 Nothobranchius populations from seasonal pools that differ in their duration to test how this parameter affects longevity and aging in two independent clades of these annual fishes.ResultsWe found that replicated populations from a dry region showed markedly shorter captive lifespan than populations from a humid region. Shorter lifespan correlated with accelerated accumulation of lipofuscin (an established age marker) in both clades. Analysis of wild individuals confirmed that fish from drier habitats accumulate lipofuscin faster also under natural conditions. This indicates faster physiological deterioration in shorter-lived populations.ConclusionsOur data provide a strong quantitative example of how extrinsic mortality can shape evolution of senescence in a vertebrate clade. Nothobranchius is emerging as a genomic model species. The characterization of pairs of closely related species with different longevities should provide a powerful paradigm for the identification of genetic variations responsible for evolution of senescence in natural populations.

Project description:BackgroundAdaptive radiations are triggered by ecological opportunity - the access to novel niche domains with abundant available resources that facilitate the formation of new ecologically divergent species. Therefore, as new species saturate niche space, clades experience a diversity-dependent slowdown of diversification over time. At the other extreme of the radiation continuum, non-adaptively radiating lineages undergo diversification with minimal niche differentiation when 'spatial opportunity' (i.e. areas with suitable 'ancestral' ecological conditions) is available. Traditionally, most research has focused on adaptive radiations, while empirical studies on non-adaptive radiations remain lagging behind. A prolific clade of African fish with extremely short lifespan (Nothobranchius killifish), show the key evolutionary features of a candidate non-adaptive radiation - primarily allopatric species with minimal niche and phenotypic divergence. Here, we test the hypothesis that Nothobranchius killifish have non-adaptively diversified. We employ phylogenetic modelling to investigate the tempo and mode of macroevolutionary diversification of these organisms.ResultsNothobranchius diversification has proceeded with minor niche differentiation and minimal morphological disparity among allopatric species. Additionally, we failed to identify evidence for a role of body size or biogeography in influencing diversification rates. Diversification has been homogeneous within this genus, with the only hotspot of species-richness not resulting from rapid diversification. However, species in sympatry show higher disparity, which may have been caused by character displacement among coexisting species.ConclusionsNothobranchius killifish have proliferated following the tempo and mode of a non-adaptive radiation. Our study confirms that this exceptionally short-lived group have diversified with minimal divergent niche adaptation, while one group of coexisting species seems to have facilitated spatial overlap among these taxa via the evolution of ecological character displacement.

Project description:BackgroundWith more than 36,000 valid fish species, teleost fishes constitute the most species-rich vertebrate clade and exhibit extensive genetic and phenotypic variation, including diverse immune defense strategies. NLRC3 subfamily genes, which are specific to fishes, play vital roles in the immune system of teleosts. The evolution of teleosts has been impacted by several whole-genome duplication (WGD) events, which might be a key reason for the expansions of the NLRC3 subfamily, but detailed knowledge of NLRC3 subfamily evolution in the family Sebastidae is still limited.ResultsPhylogenetic inference of NLRC3 subfamily protein sequences were conducted to evaluate the orthology of NLRC3 subfamily genes in black rockfish (Sebastes schlegilii), 13 other fish species from the families Sebastidae, Serranidae, Gasterosteidae and Cyclopteridae, and three species of high vertebrates (bird, reptile and amphibian). WGD analyses were used to estimate expansions and contractions of the NLRC3 subfamily, and patterns of expression of NLRC3 subfamily genes in black rockfish following bacterial infections were used to investigate the functional roles of these genes in the traditional and mucosal immune system of the Sebastidae. Different patterns of gene expansions and contractions were observed in 17 fish and other species examined, and one and two whole-genome duplication events were observed in two members of family Sebastidae (black rockfish and honeycomb rockfish, Sebastes umbrosus), respectively. Subsequently, 179 copy numbers of NLRC3 genes were found in black rockfish and 166 in honeycomb rockfish. Phylogenetic analyses corroborated the conservation and evolution of NLRC3 orthologues between Sebastidae and other fish species. Finally, differential expression analyses provided evidence of the immune roles of NLRC3 genes in black rockfish during bacterial infections and gene ontology analysis also indicated other functional roles.ConclusionsWe hypothesize that NLRC3 genes have evolved a variety of different functions, in addition to their role in the immune response, as a result of whole genome duplication events during teleost diversification. Importantly, this study had underscored the importance of sampling across taxonomic groups, to better understand the evolutionary patterns of the innate immunity system on which complex immunological novelties arose. Moreover, the results in this study could extend current knowledge of the plasticity of the immune system.

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Parallel evolution of genes controlling mitonuclear balance in short-lived annual fishes.

Publications

Parallel evolution of genes controlling mitonuclear balance in short-lived annual fishes.

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