The influence of the beginning of life on the end: A silver-spoon for senescence?

Why do indi­vidu­als vary in how quickly they age? Eve Cooper explains what her new research tells us about the effect of devel­op­ment­al envir­on­ment on senescence.

As humans, the pro­cess of sen­es­cence – exper­i­en­cing physiolo­gic­al declines as we age – is a seem­ingly ines­cap­able con­straint of our own bio­logy. But why is it that we must sen­esce? Is sen­es­cence a res­ol­ute attrib­ute of life on earth, or a mal­le­able trait, with the abil­ity to evolve – or even dis­ap­pear alto­geth­er? These ques­tions are at the root of deci­pher­ing the evol­u­tion­ary ori­gins of the age­ing process.

Up until recent dec­ades it was com­monly assumed that wild anim­als rarely exper­i­enced sen­es­cence. The argu­ment went that the risk of death from extrins­ic con­di­tions (such as pred­a­tion, star­va­tion, or expos­ure) was so high in the wild that anim­als rarely sur­vived to reach the old ages neces­sary to exper­i­ence sen­es­cence. Hence, sen­es­cence was a neg­li­gible phe­nomen­on out­side of mod­ern human soci­ety. It has only been through the long-term col­lec­tion of detailed indi­vidu­al-based data from wild anim­al pop­u­la­tions that this assump­tion has been largely dis­proven. Sen­es­cence is observed to occur in the wild across a broad range of dif­fer­ent spe­cies, and actu­ally seems to be the norm, rather than the exception.

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Female tawny owl, one of the spe­cies included in the ana­lys­is. Photo: Alex­an­dre Millon

Anoth­er fas­cin­at­ing find­ing that res­ul­ted from these long-term wild anim­al stud­ies is that there is often dra­mat­ic vari­ation between indi­vidu­als liv­ing with­in the same pop­u­la­tion in how fast or slow they sen­esce. This dis­cov­ery begs a new and import­ant ques­tion about the evol­u­tion of sen­es­cence. Assum­ing that slower sen­es­cence res­ults in high­er evol­u­tion­ary fit­ness, we should expect nat­ur­al selec­tion to wean out those with faster sen­es­cence rates, and drive evol­u­tion towards slower, poten­tially even neg­li­gible sen­es­cence in the wild. How­ever, the per­sist­ence of vari­ab­il­ity in sen­es­cence rates between indi­vidu­als indic­ates that the evol­u­tion of sen­es­cence is being inhib­ited in the nat­ur­al world. Under­stand­ing the mech­an­isms driv­ing the per­sist­ence of sen­es­cence is essen­tial in build­ing an evol­u­tion­ary frame­work through which we can under­stand ageing.

So what causes some indi­vidu­als to decline faster than oth­ers? As with many things in eco­logy, the under­ly­ing mech­an­isms have proven to be com­plex. Genes are par­tially respons­ible in determ­in­ing sen­es­cence rates – indi­vidu­als may be genet­ic­ally pre­dis­posed to decline slower or faster. Addi­tion­ally, the envir­on­ment plays a role – anim­als exposed to harsh­er con­di­tions can gen­er­ally be expec­ted to sen­esce faster. It is well estab­lished that genes and the envir­on­ment inter­act in influ­en­cing sen­es­cence rates. How­ever, it may not be only the cur­rent envir­on­ment that inter­acts with genes in affect­ing sen­es­cence rates. There is good evid­ence that the first stage of life, the devel­op­ment­al peri­od, has cru­cial influ­ence on many traits into adult­hood. For example, in humans, poor nutri­tion and stress dur­ing preg­nancy has been linked to high­er rates of car­di­ovas­cu­lar dis­ease and dia­betes in the adult life of the off­spring. In oth­er anim­al spe­cies, devel­op­ment­al envir­on­ment has been linked to adult body con­di­tion, sur­viv­al prob­ab­il­ity, and repro­duct­ive suc­cess. What if the envir­on­ment exper­i­enced dur­ing the very first stage of life, the devel­op­ment­al peri­od, has influ­ence so pro­found that it res­on­ates into the very last stage of life, influ­en­cing rates of senescence?

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Could stress dur­ing early devel­op­ment influ­ence rates of sen­es­cence in later life? Photo: Ed Uth­man, MD

The goal of our research, pub­lished today in Evol­u­tion Let­ters, was to provide a quant­it­at­ive syn­thes­is of the effects of devel­op­ment­al envir­on­ment on rates of sen­es­cence in wild anim­als. Using data from long-term stud­ies of 14 dif­fer­ent spe­cies in wild pop­u­la­tions, we con­duc­ted meta-ana­lyses to determ­ine the effect of devel­op­ment­al envir­on­ment on two dif­fer­ent types of sen­es­cence rates – sur­viv­al and repro­duct­ive sen­es­cence. The effect of devel­op­ment­al envir­on­ment was quan­ti­fied using meas­ures of nutri­tion­al avail­ab­il­ity or stress exper­i­enced dur­ing gest­a­tion or as a juven­ile, includ­ing attrib­utes of food avail­ab­il­ity, pop­u­la­tion dens­ity and weath­er conditions.

We found that, although there is no asso­ci­ation between devel­op­ment­al envir­on­ment and sur­viv­al sen­es­cence rates, there is a sig­ni­fic­ant asso­ci­ation between devel­op­ment­al envir­on­ment and repro­duct­ive sen­es­cence rates. An indi­vidu­al born into a bet­ter envir­on­ment is likely to exper­i­ence slower rates of repro­duct­ive decline in late life. This indic­ates that a high­er qual­ity devel­op­ment­al envir­on­ment can act as a pro­ver­bi­al “sil­ver-spoon”, apply­ing pos­it­ive influ­ence to the very end of life.

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The “sil­ver-spoon effect” – a high qual­ity devel­op­ment­al envir­on­ment leads to slower rates of repro­duct­ive decline in later life.

What do these res­ults mean for our broad­er under­stand­ing of the evol­u­tion of sen­es­cence? The sil­ver-spoon effect indic­ates that genes can inter­act with past envir­on­ment to influ­ence sen­es­cence. Since the influ­ence of devel­op­ment­al envir­on­ment on sen­es­cence is non-genet­ic, it has the poten­tial to weak­en the force of nat­ur­al selec­tion act­ing to slow sen­es­cence rates in the wild.  Ulti­mately, this sil­ver-spoon effect rep­res­ents a mech­an­ism that could poten­tially reduce the abil­ity of sen­es­cence to evolve. This may help explain why we see dra­mat­ic vari­ation in sen­es­cence rates between indi­vidu­als, and why sen­es­cence is not evolving in the expec­ted dir­ec­tion of slower rates and longer lifespans. A bet­ter under­stand­ing of sen­es­cence in an evol­u­tion­ary frame­work has broad import­ance, not only to evol­u­tion­ary bio­lo­gists, but as a fun­da­ment­al frame­work use­ful in all sci­entif­ic efforts to com­bat the neg­at­ive effects of sen­es­cence and improve well-being as we age.

 

Eve Cooper is a PhD stu­dent at The Aus­trali­an Nation­al Uni­ver­sity. The ori­gin­al study is freely avail­able to read and down­load here.