Abstract
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.
Highlights
Evolutionary theories of aging predict that populations which experience low extrinsic mortality evolve a retarded onset of senescence
We studied Nothobranchius populations from Southern and Central Mozambique because a striking aridity cline is present in this region
At the beginning of the dry season in 2011 and 2012, we visited sites where presence of Nothobranchius fish was detected in previous years (Reichard et al 2009; Dorn et al 2011) and recorded whether particular habitats had desiccated or not
Summary
Evolutionary theories of aging predict that populations which experience low extrinsic mortality evolve a retarded onset of senescence. 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. Evolutionary theories of aging [9,10,11] indicate that senescence is a result of age-dependent decrease in Despite enormous effort to study senescence in wild populations (reviewed in [13]) our knowledge about evolution of longevity and senescence under natural conditions in vertebrates is very limited [4,8] This is mainly because only few studies were able to employ replicated populations There is a need for resighting or recapture of the same individuals, the long lifespan of most vertebrates, the recent elucidation of more complicated predictions regarding evolution of aging, the difficulty in quantifying extrinsic mortality and several possibilities how exactly to measure senescence rate
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