Lifespan and telomere length variation across populations of wild‐derived African killifish

Abstract

Telomeres and telomerase prevent the continuous erosion of chromosome‐ends caused by lifelong cell division. Shortened telomeres are associated with age‐related pathologies. While short telomere length is positively correlated with increased lethality at the individual level, in comparisons across species short telomeres are associated with long (and not short) lifespans. Here, we tested this contradiction between individual and evolutionary patterns in telomere length using African annual killifish. We analysed lifespan and telomere length in a set of captive strains derived from well‐defined wild populations of Nothobranchius furzeri and its sister species, N. kadleci, from sites along a strong gradient of aridity which ultimately determines maximum natural lifespan. Overall, males were shorter‐lived than females, and also had shorter telomeres. Male lifespan (measured in controlled laboratory conditions) was positively associated with the amount of annual rainfall in the site of strain origin. However, fish from wetter climates had shorter telomeres. In addition, individual fish which grew largest over the juvenile period possessed shorter telomeres at the onset of adulthood. This demonstrates that individual condition and environmentally‐driven selection indeed modulate the relationship between telomere length and lifespan in opposite directions, validating the existence of inverse trends within a single taxon. Intraindividual heterogeneity of telomere length (capable to detect very short telomeres) was not associated with mean telomere length, suggesting that the shortest telomeres are controlled by regulatory pathways other than those that determine mean telomere length. The substantial variation in telomere length between strains from different environments identifies killifish as a powerful system in understanding the adaptive value of telomere length.

Protogynous functional hermaphroditism in the North American annual killifish, Millerichthys robustus

“…In this context, we identify ecological scenarios which promote such competition among females in the temporary pools inhabited by M. robustus and stimulate protogynous sex change. In natural annual killifish populations, males may become scarce later in the season 29 , 30 due to either sex-specific predation on colourful males with elaborate courtship behaviour 26 , 46 , mortality arising from male-male aggression 47 or their combination 28 . While the more conspicuous colouration and more active behaviour of male M. robustus reflect the sex differences typical of annual killifishes, the relative scarcity of males in natural populations of M. robustus , and its potential seasonal dynamics, is currently not known.…”

“…When temporary pools are filled with rainwater the embryos hatch, grow fast and mature early to produce the next generation of drought-resistant embryos before the seasonal drought. Over their adult stage, the proportion of males in the population often substantially decreases 24 , 25 due to the combined effects of sex-specific predation on the more colourful and ornamented males 26 , 27 and higher background male mortality 28 . This may lead to extremely biased sex ratios in natural populations.…”

“…This may lead to extremely biased sex ratios in natural populations. In African Nothobranchius furzeri , sex-bias in some populations may reach < 10% of males 24 , 28 and the proportion of males gradually decreases over the season in African 29 and Neotropical annual killifish 30 . Under these circumstances, the potential for protogynous sex change appears adaptive.…”

Sex chromosome differentiation via changes in the Y chromosome repeat landscape in African annual killifishes Nothobranchius furzeri and N. kadleci

“…Most biomedical and genomic research has been addressed using the model species N. furzeri, where the transcriptomic and genomic resources as well as genome editing tools have been established [34][35][36][37][38][39]. Its sister species N. kadleci Reichard, 2010 [40,41] received considerably less attention [42,43].…”

“…The studied individuals (left panel) were samples from wild-derived captive populations (for details, see [43,49–51]. Right panel: Map with geographic origin of sampled populations of N. furzeri (orange circles) and N. kadleci (green triangles) as well as N. furzeri populations studied previously by Reichwald et al [35], namely MZM-0701, MZM-0410, and GRZ of Chefu clade, and MZM-0403 of Limpopo clade (white circles).…”