Context-dependent behavioral plasticity compromises disruptive selection on sperm traits in squid

Abstract

Male animals are not given equal mating opportunities under competitive circumstances. Small males often exhibit alternative mating behaviours and produce spermatozoa of higher quality to compensate for their lower chances of winning physical contests against larger competitors [1]. Because the reproductive benefits of these phenotypes depend on social status/agonistic ranks that can change during growth or aging [2], sperm traits should be developed/switched into fitness optima according to their prospects. However, reproductive success largely relies upon social contexts arising instantaneously from intra- and inter-sexual interactions, which deter males from developing extreme traits and instead favour behavioural plasticity. Nevertheless, the extent to which such plasticity influences developmentally regulated alternative sperm traits remains unexplored. Squids of the family Loliginidae are excellent models to investigate this, because they show sophisticated alternative reproductive tactics (ARTs) by which small males, known as “sneakers”, produce longer spermatozoa and perform extra-pair copulation to attach their sperm packages near the female seminal receptacle (SR). In contrast, large “consort” males have shorter spermatozoa and copulate via pair-bonding to insert their sperm packages near the internal female oviduct [3]. In addition, plasticity in male mating behaviour is common in some species while it is either rare or absent in others. Thus, squid ARTs display a broad spectrum of adaptive traits with a complex repertoire in behaviour, morphology and physiology [3].