Sperm depletion may not limit male reproduction in a capital breeder

Abstract

Male reproduction is not only constrained by the number of encountered females but also by physiological limitations, including sperm production and the ability to sustain courtship and mating. Over a breeding season, sperm stores may drop in tandem with male energetic reserves or motivation, confounding the constraints imposed by sperm quantity with other correlated physiological limitations. We used wood frogs (Lithobates sylvaticus) to test whether explosive capital breeders are functionally limited by sperm depletion. We paired males with four conspecific females in succession and counted all of the fertilized and unfertilized eggs that each pair produced. In general, males did not experience a progressive decrease in fertilization rates with each mating (which is characteristic of sperm depletion). Instead, a few males experienced complete fertilization failure during their third and/or fourth mating, perhaps as a result of physical exhaustion, loss of motivation or hormonal changes. This pattern suggests that, even if male wood frogs do become increasingly sperm depleted over a breeding season, they are not necessarily limited by sperm. Understanding how and why fertilization rates change over multiple matings (i.e. incremental decrease vs. all-or-nothing) will help clarify the role of sperm depletion in limiting reproduction.

Reproductive output of old polygynous males is limited by seminal fluid, not sperm number

“…We found that males produced fewer offspring as they progressed through a mating sequence in Experiments A and B. Studies have previously shown that males, when multiply-mating, can become depleted of sperm and seminal fluid (Gerofotis et al, 2015;Pitnick and Markow, 1994;Rubolini et al, 2007;Sirot et al, 2009a), producing fewer offspring with females encountered later in a mating sequence (Abe, 2019;Lewis, 2004;Loyau et al, 2012;Macartney et al, 2020;Swierk et al, 2015). The asymptotic relationship between sperm stored in females, and offspring produced by females in our study, indicates that reproductive output through a mating sequence is likely limited by seminal fluid, not sperm numbers (Hopkins et al 2019b;Linklater et al, 2007;Reinhardt et al, 2011;Sirot et al, 2009a).…”

“…Ejaculate production is costly (Dowling and Simmons, 2012;Olsson et al, 1997), and males in polygynous species can become depleted of sperm (Gerofotis et al, 2015;Pitnick and Markow, 1994;Rubolini et al, 2007) and seminal fluid (Hopkins et al 2019b;Linklater et al, 2007;Reinhardt et al, 2011;Sirot et al, 2009a) when mating-multiply. Such ejaculate limitation can decrease the reproductive output of polygynous males as they progress through series of successive matings (Abe, 2019;Lewis, 2004;Loyau et al, 2012;Macartney et al, 2020;Swierk et al, 2015). In such scenarios, the effects of male reproductive senescence might become more pronounced later in a mating sequence if old males suffer steeper rates of ejaculate depletion (Bressac et al, 2008(Bressac et al, , 2009, Appendix 1).…”

Does repeated human handling of study animals during the mating season affect their offspring?

“…We captured frogs using drift fences and pitfall traps as they migrated to vernal breeding ponds. Following capture, females were weighed (“pre‐oviposition” mass measurement) and male–female pairs ( n = 50) were placed in 18‐l arenas filled with fresh pond water and covered with loose‐fitting lids (as per Swierk, Tennessen, & Langkilde, ). Arenas were arranged in groups of two around the edge of the pond; each group of two arenas was considered a trial set.…”