Parallel evolution of senescence in annual fishes in response to extrinsic mortality

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.

Community assembly inNothobranchiusannual fishes: Nested patterns, environmental niche and biogeographic history

“…Importantly, the altitudinal gradient in the study area coincides with a gradient of aridity where high‐altitude sites are significantly drier, with lower total rainfall, higher evapotranspiration rates, and lower predictability of rains (Terzibasi Tozzini et al., 2013; Vrtílek & Reichard, 2016b). The coastal plains are more humid, with temporary pools inundated for a longer period (Blažek et al., 2017; Terzibasi Tozzini et al., 2013). The flat topography of the coastal region likely connects isolated habitats with permanent water bodies more frequently than pools at a higher altitude.…”

“…Inappropriate conditions in the coastal region unlikely include a shorter duration of the dry period for embryo development, because N. furzeri and N. kadleci embryos can complete their development in less than a month (Blažek et al., 2013; Polačik, Blažek, & Reichard, 2016). Nevertheless, the more humid coastal region receives more seasonal and non‐seasonal rainfall (Blažek et al., 2017; Terzibasi Tozzini et al., 2013). It is possible that the eggs of N. furzeri and N. kadleci are more prone to non‐seasonal rains, triggering their hatching outside the appropriate season and compromising population persistence.…”

Female fecundity traits in wild populations of African annual fish: the role of the aridity gradient

“…2013). The life expectancy gradient was defined using aridity index, a ratio between the mean annual precipitation and mean annual potential evapotranspiration based on 1950–2000 averaged data (Trabucco and Zomer 2009; Fig.…”

“…The onset of seasonal rains and time of pool flooding is concordant across the region (Terzibasi Tozzini et al. 2013), but differences in precipitation and evapotranspiration lead to variation in pool duration (desiccation) along the gradient (Terzibasi Tozzini et al. 2013).…”

“…2013), but differences in precipitation and evapotranspiration lead to variation in pool duration (desiccation) along the gradient (Terzibasi Tozzini et al. 2013). Nothobranchius populations are highly genetically structured (Bartáková et al.…”