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Sperm competition is a powerful postcopulatory selective force influencing male adaptations associated with increasing fertilization success, and it is usually related to the evolution of different strategies of ejaculate expenditure between individuals. Ejaculates may also be influenced by additional selective pressures associated with sperm competition, such as timing between insemination and fertilization, female reproductive tract morphology, and fertilization environment. Also, males that adopt alternative mating tactics may face distinct sperm competition pressures, which may lead to the evolution of intraspecific diversity in ejaculates. In loliginid squids, males with alternative reproductive tactics (sneakers and consorts) differ not only in mating behavior, but also transfer spermatophores into two distinct sites within the female. Here, we compared structure and functioning of spermatophores between sneakers and consorts in the squid Doryteuthis plei applying microscopy techniques and in vitro experiments. Sneakers and consorts exhibit differences in spermatophore structure that lead to distinct spermatophoric reactions and spermatangium morphologies. Moreover, in sneakers, sperm release lasts longer and their sperm show an aggregative behavior not detected in consorts. Slow sperm release may be a strategy to guarantee longer sperm provision, given the wide interval between sneaker mating and egg release. For consorts, in turn, intense and quick sperm discharge may be advantageous, as timing between mating and egg-laying is relatively short. Within the complex squid mating system, factors such as (i) different fertilization sites and (ii) interval between mating and egg release may also influence sperm competition, and ultimately shape the evolution of divergent ejaculates between dimorphic males.

The expression of alternative reproductive tactics (ARTs) by different-sized males of loliginid squids has been extensively investigated. In loliginids, alternative phenotypes are characterized by discontinuous differences in behavior, body size, sperm deposition site, and morphology and functioning of ejaculates. Large consort males guard females, display agonistic behaviors toward rival consort males, and mate with females in the male-parallel (MP) position. Small sneaker males avoid fighting contests and instead adopt furtive behaviors to access females guarded by consort males, mating with females in the head-to-head (HH) posture. Recently, the reappraisal of preserved material from the loliginid squid Doryteuthis pleii showed that intermediate-sized males (so-called “intermediate” males) had both sneaker- and consort-like ejaculates, leading to the hypothesis of them being a transitional stage between both phenotypes. Here, we describe observations made in captivity showing that intermediate males can display agonistic behaviors toward consort males and mate with females in both mating positions, depending on the male’s current reproductive context, i.e., generally in HH, but switching to MP when the female is laying eggs. Such unusual findings of intermediate males simultaneously displaying behaviors of both sneaker and consort males comprise additional evidence corroborating the ontogenetic hypothesis for phenotypic expression of ARTs in this species. Taken together, our results indicate that (1) instead of competing with large consort males for female access and monopolization, small/young males adopt sneaker tactics to obtain mating opportunities, and (2) as they continue to grow, they gradually modify the morphology of their ejaculates and their mating behavior, going through an “intermediate” stage, before becoming large consort males.

Loliginid squids provide a unique model system to explore male alternative reproductive tactics (ARTs) and their linkage to size, behavioral decision making, and possibly age. Large individuals fight one another and the winners form temporary consortships with females, while smaller individuals do not engage in male-male agonistic bouts but use various sneaker tactics to obtain matings, each with varying mating and fertilization success. There is substantial behavioral flexibility in most species, as smaller males can facultatively switch to the alternative consort behaviors as the behavioral context changes. These forms of ARTs can involve different: mating posture; site of spermatophore deposition; fertilization success; and sperm traits. Most of the traits of male dimorphism (both anatomical and behavioral) are consistent with traditional sexual selection theory, while others have unique features that may have evolved in response to the fertilization environment faced by each temporary or permanent male morph.