Analysis of the coding sequences of clownfish reveals molecular convergence in the evolution of lifespan

Abstract

Background Standard evolutionary theories of aging postulate that reduced extrinsic mortality leads to evolution of longevity. Clownfishes of the genus Amphiprion live in a symbiotic relationship with sea anemones that provide protection from predators. We performed a survey and identified at least two species with a lifespan of over 20 years. Given their small size and ease of captive reproduction, clownfish lend themselves as experimental models of exceptional longevity. To identify genetic correlates of exceptional longevity, we sequenced the transcriptomes of Amphiprion percula and A. clarkii and performed a scan for positively-selected genes (PSGs). Results The PSGs that we identified in the last common clownfish ancestor were compared with PSGs detected in long-lived mole rats and short-lived killifishes revealing convergent evolution in processes such as mitochondrial biogenesis. Among individual genes, the Mitochondrial Transcription Termination Factor 1 ( MTERF1 ), was positively-selected in all three clades, whereas the Glutathione S-Transferase Kappa 1 ( GSTK1 ) was under positive selection in two independent clades. For the latter, homology modelling strongly suggested that positive selection targeted enzymatically important residues. Conclusions These results indicate that specific pathways were recruited in independent lineages evolving an exceptionally extended or shortened lifespan and point to mito-nuclear balance as a key factor. Electronic supplementary material The online version of this article (10.1186/s12862-019-1409-0) contains supplementary material, which is available to authorized users.

Cophylogenetic analysis of the relationship between anemonefish Amphiprion (Perciformes: Pomacentridae) and their symbiotic host anemones (Anthozoa: Actiniaria)

“…In this association, the benefits for the anemonefish include protection from predators , removal of external parasites , gaining additional nutrients from tentacles, and increase in reproductive fitness through egg protection Saenz-Agudelo et al 2011). Anemonefish are long-lived, and are used as an experimental model of exceptional longevity Sahm et al 2019). Their lifespan is generally more than 30 years.…”

Membrane peroxidation index and maximum lifespan are negatively correlated in fish of genus Nothobranchius

“…aridity) strictly limits the natural lifespan of Nothobranchius fishes in the wild (Tozzini et al, 2013), this short lifespan is retained under captive conditions and is coupled to rapid expression of a host of conserved age-associated phenotypes (Cellerino et al, 2016). In addition, the genus Nothobranchius evolved from a non-annual (therefore, longerlived) ancestor, the sister genus Aphyosemion (Sahm et al, 2019) and the two taxa provide a sharp phenotypic contrast.…”

Anemonefish, a model for Eco-Evo-Devo

“…The lifespan of A. percula has been estimated to be about 30 years [34]. Sahm and collaborators (2019) performed a survey of anemonefish lifespan data in the wild and in captivity, in which they identified at least two additional species (A. ocellaris and A. melanopus) with a lifespan of over 20 years [35]. Because this lifespan is longer than other teleost fish of the same size, anemonefish could become an experimental model for long-lived vertebrates [34].…”

“…Because this lifespan is longer than other teleost fish of the same size, anemonefish could become an experimental model for long-lived vertebrates [34]. For example, recently, anemonefish have been used to understand the genetic architecture underlying differences in lifespan [35]. Taking advantages of the transcriptome of 5 anemonefish species, Sahm et al (2019) identified genes that underwent accelerated molecular evolution in association with the evolution of a long lifespan [35].…”