An Ecology of Sperm: Sperm Diversification by Natural Selection

Abstract

Using basic ecological concepts we introduce sperm ecology, a framework to study sperm cells.We first describe environmental effects on sperm and conclude that evolutionary and ecological research should not neglect the overwhelming evidence presented here (both in external and internal fertilizers, and in terrestrial and aquatic habitats) that sperm function is altered by many environments, including the male environment. Second, we conclude that the evidence for sperm phenotypic plasticity is overwhelming. Third, we find that genotype-by-environment interaction effects on sperm function exist but their general adaptive significance (e.g. local adaptation) awaits further research. It remains unresolved whether sperm diversification occurs by natural selection acting on sperm function, or on male and female micro-environments that enable optimal plastic performance of sperm ('sperm niches'). Environmental effects reduce fitness predictability under sperm competition, predict species distributions under global change, explain adaptive behavior, and highlight the role of natural selection in behavioral ecology and reproductive medicine. Adriaenssens B, van Damme R, Seebacher F, Wilson RS. 2012. Sex cells in changing environments: can organisms adjust the physiological function of gametes to different temperatures? Global Change Biol. 18:1797-1803 Aitken, RJ. 2006. Sperm function tests and fertility. Int. J. Androl. 29:60-75 Aitken RJ, Baker MA 2013. Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int. J. Dev. Biol. 57:265-72 Aitken, R. J. & Clarkson, J. S. (1988) Significance of reactive oxygen species and anti-oxidants in defining the efficacy of sperm preparation techniques. J Androl 9:367-76 Aitken RJ & Koppers AJ. (2011) Apoptosis and DNA damage in human spermatozoa. Asian J Androl 13:36-42 Aitken RJ, De Iuliis GN, McLachlan RI. 2009. Biological and clinical significance of DNA damage in the male germ line. Int. J Androl. 32:46-56 Aitken RJ, Gibb Z, Mitchell LA, Lambourne SR, Connaughton HS, De Iuliis GN. 2012. Sperm motility is lost in vitro as a consequence of mitochondrial free radical production and the generation of electrophilic aldehydes but can be significantly rescued by the presence of nucleophilic thiols. Biol. Reprod. 87:110 Aitken RJ, Bronson R, Smith TB, De Iuliis GN. The source and significance of DNA damage in human spermatozoa; a commentary on diagnostic strategies and straw man fallacies. Mol Hum Reprod 2013; 19: 475-85 Aitken RJ, Smith TB, Jobling MS, Baker MA, De Iuliis GN. 2014. Oxidative stress and male reproductive health. Asian J. Androl. 16:31-8 Alavi SMH, Cosson J. 2005. Sperm motility in fishes. i. Effects of temperature and ph: a review.

Post‐ejaculatory modifications to sperm (PEMS)

“…Each sex‐specific trait can theoretically generate selection on the other (i.e. coevolution) as a consequence of both natural/ecological selection (Reinhardt, Dobler, & Abbott, ) and post‐copulatory sexual selection (Birkhead, Møller, & Sutherland, ; Keller & Reeve, ; Eberhard, ; Yasui, ; Snook, ; Pitnick, Wolfner, & Suarez, ; Orr & Brennan, ; Firman et al ., ; Lüpold & Pitnick, ). There is also some empirical evidence, albeit limited, suggesting that FRT design may evolve first, with sperm form then evolutionarily tracking such changes (i.e.…”

Developmental diet irreversibly shapes male post‐copulatory traits in the neriid fly Telostylinus angusticollis

“…Male post‐copulatory traits, such as sperm and semen traits, can be highly susceptible to changes in the male environment (reviewed in Reinhardt et al ., ). For example, a reduction in nutrient availability often results in a decrease in post‐copulatory trait expression (e.g.…”

“…Perry & Rowe, ; Mehlis et al ., ), perhaps because low condition males tend to have reduced mating success, and may therefore strategically invest their limited resources into sperm and ejaculate traits to make the most of any mating opportunities that arise (Parker, ; Williams et al ., ; Cameron et al ., ; Parker & Pizzari, ). These differences among studies likely reflect species differences in reproductive ecology (Simmons et al ., ; Cornwallis & Birkhead, ; Reinhardt et al ., ). However, another factor that is often overlooked is the timing of nutritional restriction.…”

More Pitfalls with Sperm Viability Staining and a Viability-Based Stress Test to Characterize Sperm Quality

“…In addition to these conceptual issues, Holman (2009), reviewing the use of SV in ecology and evolution, identified additional technical problems: (1) because the SV assay itself causes sperm mortality, the "true" number of live and dead sperm cannot be known. (2) Given the wide-ranging environmental effects on sperm quality (Reinhardt et al, 2015), sperm from different organs or at different cellular ages may have different membrane properties. Comparing their SV may therefore be confounded by different amounts of sperm being killed during dissection and during staining.…”

“…Comparing their SV may therefore be confounded by different amounts of sperm being killed during dissection and during staining. Given the rapid evolutionary change in sperm form (Pitnick et al, 2009) and sperm function (Reinhardt et al, 2015), different species may differ in both in SV as well as its susceptibility to the staining dye. (3) Both in nature and on the microscopic slide, SV may not be independent of the total number of sperm.…”