Why small males have big sperm: dimorphic squid sperm linked to alternative mating behaviours

BACKGROUND: Sperm cells are the target of strong sexual selection that may drive changes in sperm structure and function to maximize fertilisation success. Sperm evolution is regarded to be one of the major consequences of sperm competition in polyandrous species, however it can also be driven by adaptation to the environmental conditions at the site of fertilization. Strong stabilizing selection limits intra-specific variation, and therefore polymorphism, among fertile sperm (eusperm). Here we analyzed reproductive morphology differences among males employing characteristic alternative mating behaviours, and so potentially different conditions of sperm competition and fertilization environment, in the squid Loligo bleekeri. RESULTS: Large consort males transfer smaller (average total length = 73 μm) sperm to a female's internal sperm storage location, inside the oviduct; whereas small sneaker males transfer larger (99 μm) sperm to an external location around the seminal receptacle near the mouth. No significant difference in swimming speed was observed between consort and sneaker sperm. Furthermore, sperm precedence in the seminal receptacle was not biased toward longer sperm, suggesting no evidence for large sperm being favoured in competition for space in the sperm storage organ among sneaker males. CONCLUSIONS: Here we report the first case, in the squid Loligo bleekeri, where distinctly dimorphic eusperm are produced by different sized males that employ alternative mating behaviours. Our results found no evidence that the distinct sperm dimorphism was driven by between- and within-tactic sperm competition. We propose that presence of alternative fertilization environments with distinct characteristics (i.e. internal or external), whether or not in combination with the effects of sperm competition, can drive the disruptive evolution of sperm size

Male alternative reproductive tactics and associated evolution of anatomical characteristics in loliginid squid

© The Author(s), 2019. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Marian, J. E. A. R., Apostólico, L. H., Chiao, C. C., Hanlon, R. T., Hirohashi, N., Iwata, Y., Mather, J., Sato, N., & Shaw, P. W. Male alternative reproductive tactics and associated evolution of anatomical characteristics in loliginid squid. Frontiers in Physiology, 10, (2019): 1281, doi: 10.3389/fphys.2019.01281.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.JM acknowledges the funding provided by FAPESP (São Paulo Research Foundation – proc. 2013/02653-1, 2014/11008-5, 2015/15447-6, 2017/16182-1, and 2018/19180-2), CNPq (National Council for Scientific and Technological Development – proc. 477233/2013–9), and CAPES (Coordination for the Improvement of Higher Education Personnel – Finance Code 001)

Video imaging of the sperm acrosome reaction during in vitro fertilization

Mammalian spermatozoa become competent for fusion with oocytes while traveling through the female reproductive tract and the oocyte's extracellular investments. Recent studies highlighted the molecular mechanism of the sperm's interactions with the zona pellucida (ZP), the extracellular coat surrounding the oocyte. Fertilizing spermatozoa initiate the sperm acrosome reaction (AR), essential for zona penetration and fusion with the oocyte plasma membrane, before they reach the ZP. However, the exact condition of spermatozoa that leads to successful penetration of the ZP remains unknown. We performed microscopic observations of in vitro fertilization with genetically (EGFP) and chemically (antibody and lectin) labeled spermatozoa to monitor the progression of the AR. Spermatozoa exhibiting EGFP−/PNA+ prior to binding to the ZP initiated zona penetration. This result suggests that spermatozoa that have undergone the AR are still capable of binding and penetrating the ZP

Unresolved questions concerning mammalian sperm acrosomal exocytosis

In recent years, the study of mammalian acrosomal exocytosis has produced some major advances that challenge the long-held, general paradigms in the field. Principally, the idea that sperm must be acrosome-intact to bind to the zona pellucida of unfertilized eggs, based largely on in vitro fertilization studies of mouse oocytes denuded of the cumulus oophorus, has been overturned by experiments using state-of-the-art imaging of cumulus-intact oocytes and fertilization experiments where eggs were reinseminated by acrosome-reacted sperm recovered from the perivitelline space of zygotes. In light of these results, this minireview highlights a number of unresolved questions and emphasizes the fact that there is still much work to be done in this exciting field. Future experiments using recently advanced technologies should lead to a more complete and accurate understanding of the molecular mechanisms governing the fertilization process in mammals.Fil: Buffone, Mariano Gabriel. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental (i); ArgentinaFil: Hirohashi, Noritaka. Shimane University. Education and Research Center for Biological Resources; JapónFil: Gerton, George L.. University Of Pennsylvania; Estados Unido