Actuarial senescence in a long-lived orchid challenges our current understanding of ageing

Abstract

The dominant evolutionary theory of actuarial senescence-an increase in death rate with advancing age-is based on the concept of a germ cell line that is separated from the somatic cells early in life. However, such a separation is not clear in all organisms. This has been suggested to explain the paucity of evidence for actuarial senescence in plants. We used a 32 year study of Dactylorhiza lapponica that replaces its organs each growing season, to test whether individuals of this tuberous orchid senesce. We performed a Bayesian survival trajectory analysis accounting for reproductive investment, for individuals under two types of land use, in two climatic regions. The mortality trajectory was best approximated by a Weibull model, showing clear actuarial senescence. Rates of senescence in this model declined with advancing age, but were slightly higher in mown plots and in the more benign climatic region. At older ages, senescence was evident only when accounting for a positive effect of reproductive investment on mortality. Our results demonstrate actuarial senescence as well as a survival-reproduction trade-off in plants, and indicate that environmental context may influence senescence rates. This knowledge is crucial for understanding the evolution of demographic senescence and for models of plant population dynamics.

Demographic senescence and effects on population dynamics of a perennial plant

“…Our results are interesting in the context of understanding general patterns of aging in plants, in that they corroborate findings of a few recent detailed studies that report evidence of actuarial senescence (Pico and Retana 2008, Roach et al 2009, Dahlgren et al 2016b), but also show substantial differences among populations. That plants show actuarial senescence is in line with predictions of classical evolutionary theories of aging, i.e., that no organism can escape senescence (Hamilton 1966).…”

“…, Dahlgren et al. ), but also show substantial differences among populations. That plants show actuarial senescence is in line with predictions of classical evolutionary theories of aging, i.e., that no organism can escape senescence (Hamilton ).…”

“…Roach et al 2009). For example, the site with a constant decrease in survival is more disturbed by both wind and cattle than the other sites, and high survival at low ages can be expected to be advantageous in such environments, even if it comes at a cost of lower survival of older plants (e.g., Dahlgren et al 2016b). We also found evidence of effects of heterogeneity of individual frailty (Vaupel and Yashin 1985), in terms of increasing average survival at very old ages, but only at the site with the highest overall survival.…”

“…, Dahlgren et al. , Quarles and Roach ). It has been suggested that some plants may even show “negative senescence,” an increasing survival probability after the onset of reproduction (Vaupel et al.…”

“…However, the long-term studies that do exist show conflicting results regarding how age affects fecundity and survival. Several studies indicate no or negligible senescence in plants (Harper and White 1974, Rose et al 1998, Hutchings 2010, Dahlgren et al 2016c, but there are also recent studies that have found evidence of demographic senescence (Pico and Retana 2008, Roach et al 2009, Dahlgren et al 2016b, Quarles and Roach 2018. It has been suggested that some plants may even show "negative senescence," an increasing survival probability after the onset of reproduction (Vaupel et al 2004).…”