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| Author(s): |
Lígia Haselmann Apostolico
Total Authors: 1
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| Document type: | Doctoral Thesis |
| Press: | São Paulo. |
| Institution: | Universidade de São Paulo (USP). Instituto de Biociências (IBIOC/SB) |
| Defense date: | 2023-08-28 |
| Examining board members: |
José Eduardo Amoroso Rodriguez Marian;
Solimary Garcia Hernandez;
Flávio Dias Passos
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| Advisor: | José Eduardo Amoroso Rodriguez Marian |
| Abstract | |
Sexual selection inflicts a major influence on males reproductive success, and it is not limited to a simple competition for female monopolization. When females mate with several partners during their reproductive season, the dispute over offspring paternity can persist even after mating, through mechanisms of sperm competition and cryptic female choice. Evidence from innumerous taxa has also demonstrated how, not uncommonly, post-copulatory sexual selection shapes the evolution of male adaptations in terms of behavior, morphology, or physiology in ways to maximize the success of their sperm over those of rival males. Mate guarding behavior, transferring seminal fluids capable of reducing female receptivity, and mating plugs, for instance, are classical examples of such adaptations, often related to males attempts to minimize sperm competition. Under fierce male-male competition for oocyte fertilization, males may also maximize their chances of success by optimizing sperm production, in terms of sperm quantity or even quality (e.g., viability, velocity attributes). Loliginidae squids exhibit highly complex mating behaviors; polygamy, sperm competition, and multiple paternity are common phenomena in this family. Moreover, different-sized males often display opposite behaviors (i.e., alternative reproductive tactics) to acquire female partners and ultimately oocyte fertilization. Larger males, known as consorts, display agonistic behaviors and mate-guarding to protect their female partners from the harassment of other consorts. They place themselves under the female and mate in the so-called male-parallel position, placing their spermatophores inside the females mantle cavity, near the oviduct opening. In contrast, smaller males, known as sneakers, do not engage in aggressive behaviors nor protect their partners; instead, they mate surreptitiously with females guarded by consorts. They place themselves in front of the female and mate in the so-called head-to-head position, attaching their ejaculates at the females buccal membrane, near the seminal receptacle a sac-like structure responsible for long-term sperm storage. Previous studies on loliginids have commonly suggested that males using different mating positions should have highly unequal reproductive success, given the spatial differences between the fertilization site (oviducal membranes, more internal; buccal membrane, more external) used by each male phenotype. Empirical evidence supporting such predictions was, however, still lacking. Using the loliginid Doryteuthis pleii (Blainville, 1823) as a model, the primary goal of this Thesis aimed at understanding the reproductive success of each male phenotype when their gametes, located at spatially distinct fertilization sites, compete over the same set of oocytes. By conducting mating trials in captivity and genotyping a large set of the resulting embryos using microsatellite markers, the present outcomes have revealed that, as expected, males whose sperm is located more internally typically monopolize offspring fertilization (paternity rate: > 92%) when competing with sperm stored in the more external site, probably due to the privileged access of their sperm to non-fertilized oocytes freshly released from the oviduct opening. However, even in such scenarios, sneaker males might also sire a considerable share of the remaining oocytes (paternity rate: 0.7 8 %). Combining such outcomes with our data on the genetic variability of stored sperm from wild females (minimum number of males: 3.0 ± 1.37), the present results highlight the importance of the seminal receptacle in loliginids. By providing additional sperm for females, the storage organ does not only play a fundamental role in the fertilization dynamics and genetic variability of females offspring but also in the maintenance of the sneaker tactic along different generations. By providing long-term sperm storage, the seminal receptacle allows sneakers to gain a cumulative reproductive success, even allocating fewer ejaculates per female (i.e., by investing less sperm per female, they can mate with a higher number of females). Long-term sperm storage may also promote intense sperm competition between sneaker males. In agreement with such an idea, a previous study on D. pleii has suggested that sneakers could transfer putative mating plugs to the female seminal receptacle, capable of physically obstructing its narrow opening and, consequently, preventing her from using her sperm reserve. By comparing the paternity rates obtained by unknown sneakers (i.e., whose sperm had been stored before female capture) when in the presence or absence of spermatangia attached inside the seminal receptacle, the present outcomes indeed revealed a possible function of these structures as effective mating plugs (paternity rates of unknown males, with mating plugs: 0.9 ± 0.8 %; without mating plugs: 28.1 ± 40.9 %; p = 0.134; number of unknown sires, with mating plugs: 0.7 ± 0.6; without mating plugs: 2.2 ± 1.6; p = 0.216). Nevertheless, while mating plugs may have arisen as an adaptation to the intense sperm competition faced by sneakers, it is not inconceivable to speculate that females might also influence their efficiency, given the conflict of interests between sexes imposed by these structures. And finally, by applying both light and transmission electron microscopy techniques, we focused on the morphology of the hectocotylus, responsible for transferring spermatophores to the female during mating and therefore an important structure to cephalopod reproduction. Our analyses revealed the existence of two secretory cell types, exclusively found in the left ventral arm of males. We speculate that both cell types act together to produce a viscous secretion that helps gripping the spermatophores during mating. Combined, the seven chapters of the present Thesis provide important contributions to post-copulatory sexual selection, highlighting the fundamental role of the fertilization environment when studying the fertilization dynamics, males reproductive success, and evolution and maintenance of male intrasexual dimorphism in species with alternative reproductive tactics. (AU) | |
| FAPESP's process: | 17/16182-1 - Post-copulatory sexual selection in a squid (Mollusca: Cephalopoda) with male intrasexual dimorphism and two fertilization sites |
| Grantee: | Lígia Haselmann Apostólico |
| Support Opportunities: | Scholarships in Brazil - Doctorate |