Abstract
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.
Highlights
Mating behavior of loliginid squids (Loliginidae, Cephalopoda) is notable because they exhibit several complex behaviors, including agonistic contests and mate guarding (Hanlon and Messenger, 2018), and because, for several species, males within the same population can express alternative reproductive tactics (ARTs) when pursuing the fertilization of females’ ovaMale Behavior Supports Ontogenetic Phenotypes (Supplementary Figure S1) (e.g., Hanlon, 1996; Hanlon et al, 2002; Iwata et al, 2005)
Raw data from each experiment, including information on spermatophore and spermatangia morphology obtained from dissected males and females, respectively, are presented in Supplementary Tables S1–S3
Aggressive demonstrations advertised by males often started with the exhibition of typical skin colorations, such as the pattern known as “all dark” and the display of “lateral flames” and “mid-ventral ridge” along the body (Supplementary Figure S1D and Figures 1A–C), usually progressing to actual physical disputes, such as “fin-beating”
Summary
Mating behavior of loliginid squids (Loliginidae, Cephalopoda) is notable because they exhibit several complex behaviors, including agonistic contests and mate guarding (Hanlon and Messenger, 2018), and because, for several species, males within the same population can express alternative reproductive tactics (ARTs) when pursuing the fertilization of females’ ovaMale Behavior Supports Ontogenetic Phenotypes (Supplementary Figure S1) (e.g., Hanlon, 1996; Hanlon et al, 2002; Iwata et al, 2005). Female guarding occurs before and after mating and while the female is laying eggs (Hanlon et al, 1997; Hanlon, 1998) It consists of a series of agonistic exhibitions toward rival males, including the expression of stereotyped body patterns (e.g., the exhibition of red stripes laterally along the body, referred as “lateral flames”) (Supplementary Figure S1D) and even the engagement in physical bouts with other consort males (DiMarco and Hanlon, 1997). During mating, they place themselves below the females and mate with them in a position called “male-parallel” (MP), inserting their spermatophores inside the female’s body and implanting them near her oviduct opening (Supplementary Figures S1A,E,F). They place themselves in front of the female and mate with her in a position known as “head-to-head” (HH), usually without any resistance from consort males, placing their spermatophores near the seminal receptacle of the female, located close to her mouth region (Supplementary Figures S1A–C) (e.g., Hanlon, 1996; Hanlon et al, 1997)
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