Sex, senescence, sources and sinks

Why do most organisms age, and why do most of them reproduce sexually? Does sex rejuvenate? We review progress that has been made linking theories of senescence with those of sexual reproduction. We show that there is a dearth of theory against the numerous questions waiting to be answered theoretically or empirically: observed senescence patterns are a result of past selection acting on individuals of different age categories and abundances, modes of reproduction (asexual, sexual, facultatively sexual, via buds or zygotes). Modular organisms present their own challenges. Assigning offspring an unambiguous age of zero at birth is often too simplistic. We also comment on germline mutations as a form of ageing over generations (Lansing effect) and ask whether there is value in reinvigorating an old metaphor (1988, Sex and death in the protozoa. New York, NY, USA: Cambridge University Press) of chairs and their chairmakers who both are subject to deterioration over time, since endogenous repair is never foolproof. Future theory could usefully revisit a known mathematical analogy between selection on senescence across age classes and source-sink theory. Some modes of reproduction (particularly asexuality) may yield offspring that are, in a sense, already aged, with the problem increasing over generations (ultimately leading to a demographic sink). Insofar as sexuality 'rejuvenates', it does so through a gamble that, with some frequency, produces 'exogenously repaired' individuals that act as a source of genes to future generations. This gamble has been argued to be managed best when life cycles include a unicellular stage (zygote), an argument that could be usefully complemented with an analysis of the relevant economic trade-offs between offspring size and number. A free Plain Language Summary can be found within the Supporting Information of this article.