Male fattening is related to increased seminal quality of squirrel monkeys (Saimiri collinsi): Implications for sperm competition

Abstract

Saimiri are neotropical primates with seasonal reproduction, males develop a seasonal fattening condition that has been suggested as a pre-copulatory sexual selection strategy. Furthermore, females mate with multiple males in the same season. This could also favor the evolution of a postcopulatory sexual strategy by sperm competition. In this study, we tested the hypothesis that there is a relationship between the fatted condition and advantageous seminal characteristics in Saimiri collinsi and evaluated its implications for sperm competition. Adult males (N = 10), aged 5-15 years, housed in mixed or only-male groups, were analyzed from June, 2015 to July, 2016. Measurements of weight, axilla, and arm skinfold, and testicular volume were taken monthly, and semen was collected by electroejaculation. A fattening index was developed to quantify and identify fatted males, biometrics, and seminal parameters were compared between the non-fatted and fatted conditions.The fatted males present a larger testicular volume. This is related to the increase in spermatogenic activity necessary to sustain a high ejaculation frequency during the mating season. An increase in seminal volume and in frequency of semen coagulation were detected in fatted males, advantages related to sperm protection in the female reproductive tract. Age and social context were not significant sources of variation for both morphological and seminal traits. A decrease in response from the fatted males in obtaining semen and an increase in the frequency of azoospermic ejaculates were observed. These unexpected results may be due to intense reproductive activities in a short period. The fattening phenomenon has many implications in the sexual selection of squirrel monkeys, and they are still not entirely unveiled. Our results corroborate the idea that, in S. collinsi, the fatted male condition is related to sexual selection, and we found evidence suggesting it may be also expressed by a post-copulatory component, sperm competition.

Seasonal variations in gonadosomatic index and seminal quality of squirrel monkeys (Saimiri collinsi)

“…42 Since we did not control copulation in this study, there is a high probability that some of the males ejaculated before semen collection. This would result in a decrease in the sperm concentration in these samples, as also suggested by Sampaio et al, 25 A period of sexual abstinence has a positive influence on sperm concentration but a negative impact on motility, plasma membrane functionality and integrity, DNA fragmentation, and mitochondrial damage. 43,44 This may be due to the high content of polyunsaturated fatty acids (PUFAs), which make sperm membranes very sensitive to lipid peroxidation.…”

“…This may be the result of the increased sperm production required when ejaculates from different males cooccur and compete for opportunities to fertilize oocytes, which will be available at a restricted time of year when females ovulate. 4,40 Sampaio et al 25…”

“…38 The hormones on the sex glands, stimulate the secretion of sufficient seminal fluid to suspend sperm and maintain viability. This activity causes vaginal pH buffering 6 and may be a response to the increased need for semen coagulation 25 which, in turn, may favor the survival of spermatozoa in the female's reproductive tract until the time of ovulation, increasing the chances of fertilization. This demonstrates the advantages of sperm protection and may be related to sperm competition mechanisms, discussed for the same animal groups that exhibit seasonal fattening.…”

“…This demonstrates the advantages of sperm protection and may be related to sperm competition mechanisms, discussed for the same animal groups that exhibit seasonal fattening. 25 The GSI cannot be used as an index to predict sperm quality.…”

“…17 In free-living or semicaptive squirrel monkeys (S. sciureus and S. collinsi), seasonal fattening is associated with the activation of spermatogenesis and testis enlargement. 16,[23][24][25] In captivity, seasonality may persist or not, 26 and reproductive cycle patterns are widely divergent. 27 This makes it difficult to select the best semen donors, determine the best period for semen collection, establish mating or artificial insemination stations, and optimize other assisted reproduction techniques.…”