Evidence for adaptive explanations of semelparity in animals

Semelparity, the reproductive strategy of reproducing once, is widespread but uncommon in animals. Classes of models to explain the evolution of semelparity are based either on age structure and mortality schedules - demographic models in which high post-reproductive mortality risk favours high reproductive effort and semelparity results from survival costs of reproduction - or on optimal allocation of reproductive effort. We review and synthesise evolutionary explanations for the life history strategy of semelparity in animals. We find that semelparity has been reported in around 5000 of the one million named metazoan species (around 0.5%), and, including the 930 cephalopod species, explanations for semelparity have been proposed for around 1020 species, including 30 species with semelparity only in males. Phylogenetic regressions that can test the predictions of competing models to explain semelparity have been applied to four groups of animals: dasyurid and didelphid marsupials, salmonid fish, forficulid insects, and the spider families Nephilidae, Araneidae, Theridiidae, and Dolomedidae. These tests support the demographic model in taxa with semelparous females. The major drivers of post-reproductive mortality risk that are associated with the evolution of semelparity in animals are risky and energetically demanding breeding migration, particularly to the deep ocean, and seasonally harsh climates in which periodic food shortage restricts reproductive opportunities. Species with semelparity only in males share a set of reproductive traits that appear contradictory. They cease sperm production at maturity, yet use fatal forms of mate-guarding for paternity protection that suggest intense sperm competition, such as tearing off body parts to plug the female opening (spiders and insects) or catabolising muscle to fuel prolonged, repeated mating effort (mammals). Comparative tests suggest that post-mating sexual selection under sexual conflict is the driver in animals with male-only semelparity, consistent with reproductive effort models that require no environmental factor to raise post-reproductive mortality. We propose a new explanation for the loss of sperm production ability at maturity in species with male-only semelparity: that this is an adaptation to intense sperm competition associated with extreme reproductive effort in males.