The Editor’s Choice paper for issue 5 is a study on the variation in senescence across different strains of duckweed by Patrick Barks and colleagues. Rob Salguero-Gómez, who handled the paper as an Associate Editor, has given some thoughts on the significance of the work.
One could say that modern human societies are slaves to the clock. Just think about it: how many times do you check the time on a daily basis? Indeed, time matters to us… but does it to other creatures?
At a lower temporal resolution, say years, time dictates to a large extent when we send our children to kindergarten, when they enter primary school and graduate from high-school, when we get our first job (+/- a large standard variation, admittedly), buy a house, get married/couple up, retire, and (just as a matter of time itself, together with other factors such as behaviour [Lin, 2018] and socio-economic background [Robertson et al., 2012]), when death hits us.
Time is a human invention which we are most intimately acquainted. Yet, other species like the magnificent bristlecone pine (Pinus longaeva) and its world record of over 4,700 years of longevity (Lanner & Connor, 2001), probably not so much. Why so?
For one thing, those of us humans lucky enough to have overcome the boundary of 30 years of age will have started to notice some changes in anatomic and physiological performance. You don’t feel quite as good after a night as you used to, huh? Senescence, i.e. the decay of anatomic and physiological functions, decline in fertility and/or increase in the risk of mortality with age, is one of the hallmarks of being a human. This is so despite the fact that we have achieved a remarkable extension of lifespan in the last 200 years (Colchero et al., 2016). In fact, similar patterns of increase in mortality risk and decline in fertility have been reported in many mammals and birds… but how about the tree of life?
A few years ago, senescence was shown to be the exception (Jones et al., 2014) rather than the rule as theoretical predictions had stated (Medawar, 1946, 1952; Williams, 1957; Kirkwood, 1977). It was shown that, in fact, quite a few animals, including hydra (Hydra magnipapillata), some birds like the southern fulmar (Fulmarus glacialoides), and many plant species show patterns that either do not quite match predictions, or completely oppose to them. For instance, in Scots pines (Pinus sylvestris) and freshwater crocodile (Crocodylus johnsoni) fertility increases with age, whereas in the oarweed (Laminaria digitata) and desert tortoise (Gopherus agassizii) fertility increases to a plateau level and the risk of mortality declines with age.
The focus in ageing research since then has shifted from “what causes senescence?” to a more comprehensive research agenda that now also asks “why do some species senesce and others do not?” This shift means that a trait such as senescence is now finally understood as a characteristic with inter-specific variation. And I say “finally” because to any researcher carrying out demographic research on perennial plants, or anybody walking around 300 year old French vineyards, the fact that senescence is not universal will come as anything but news.
What the field needs now, is a mechanistic understanding of the sources of variance behind age-based trajectories of fitness components: survival and reproduction. That is precisely what is done in a recent publication by Dr Patrick Barks and colleagues titled, Among‐strain consistency in the pace and shape of senescence in duckweed, which has been selected as the editor’s choice of Journal of Ecology’s latest issue (106.5).
In their paper, the authors explore variation in senescence across strains of 1,700 individuals of duckweed (Lemna turionifera) across 25 sites in Canada. In order to make fair comparisons across sites, where age at maturity and mean life expectancy can vary widely, they standardised the moments of longevity and rate of senescence using the concepts of pace and shape, respectively, as first developed by Pearl & Miner (1935), Demetrius (1974, 1978), Keyfitz (1977), and more recently improved by Baudisch et al. (2013).
Pace is a metric that informs on the length of life and survival and reproductive events in units of absolute time, whereas shape is a dimensionless metric that informs on the direction and magnitude of changes in mortality or fecundity as individuals from a cohort age. Thus, shape trajectories that approximate a concave (down) curve are said to detect senescence. This is so because, in them, more individuals die at advanced ages, consistent with the decline in function that is attributed to senescence.
Barks and colleagues found overwhelming evidence for age-related increases in the risk of mortality and declines in fecundity, but with mortality decelerating and eventually plateauing at advanced ages. In other words, duckweed strains senesced for fertility, but underwent negligible senescence (sensu, Vaupel et al., 2014) for survival. Their research highlights that exploring only one fitness function (either survival or fertility) does not provide a complete picture on the ability of the organism to escape from or evolve senescence. Interestingly, the measures of pace and shape did not vary much across sites, suggesting that the metrics that describe age-based performance in duckweed may be fixed at the species level, and not much affected by the environment, as quantified in terms of temperature, nutrient concentration and salinity.
Two of the most widely cited theories of the evolution of senescence, antagonistic pleiotropy theory (Williams, 1957) and disposable soma (Kirkwood, 1977), are founded upon the concept of trade-offs. In simple words: individuals senesce because of compromises between vital functions. While there is evidence at the inter-specific level that trade-offs between survival, development and reproduction correlate with the chances of an organism to escape from senescence (Salguero‐Gómez, 2017; Salguero‐Gómez & Jones, 2017), Bark and colleagues found no evidence at the intra-specific level.
Ageing research is a rather prolific branch of science. A quick search of the terms “senescence” in ISI Web of Knowledge will output over 3 million peer-review publications on the topic. However, a lot of this research has focused on human populations and non-human, animal populations. The research focus beyond mammals and birds has remained scant, though of course exceptions exist, such as a Journal of Ecology Special Feature a few years back.
This publication by Barks et al. constitutes a critical step forward in population ecology, ageing research and evolutionary biology due to their elegant methodology, novel angle on intra-specific variation coupled with variance decomposition of potential environmental drivers and extensive sample size.
Rob Salguero-Gómez, University of Oxford, UK
Read the full paper online: Among‐strain consistency in the pace and shape of senescence in duckweed