Beyond Testis Size: Links between Spermatogenesis and Sperm Traits in a Seasonal Breeding Mammal

Abstract

Spermatogenesis is a costly process that is expected to be under selection to maximise sperm quantity and quality. Testis size is often regarded as a proxy measure of sperm investment, implicitly overlooking the quantitative assessment of spermatogenesis. An enhanced understanding of testicular function, beyond testis size, may reveal further sexual traits involved in sperm quantity and quality. Here, we first estimated the inter-male variation in testicular function and sperm traits in red deer across the breeding and non-breeding seasons. Then, we analysed the relationships between the testis mass, eight parameters of spermatogenic function, and seven parameters of sperm quality. Our findings revealed that the Sertoli cell number and function parameters vary greatly between red deer males, and that spermatogenic activity co-varies with testis mass and sperm quality across the breeding and non-breeding seasons. For the first time in a seasonal breeder, we found that not only is the Sertoli cell number important in determining testis mass (r = 0.619, p = 0.007 and r = 0.248, p = 0.047 for the Sertoli cell number assessed by histology and cytology, respectively), but also sperm function (r = 0.703, p = 0.002 and r = 0.328, p = 0.012 for the Sertoli cell number assessed by histology and cytology, respectively). Testicular histology also revealed that a high Sertoli cell number per tubular cross-section is associated with high sperm production (r = 0.600, p = 0.009). Sperm production and function were also positively correlated (r = 0.384, p = 0.004), suggesting that these traits co-vary to maximise sperm fertilisation ability in red deer. In conclusion, our findings contribute to the understanding of the dynamics of spermatogenesis, and reveal new insights into the role of testicular function and the Sertoli cell number on testis size and sperm quality in red deer.

Intramale variation in sperm size: functional significance in a polygynous mammal

“…It is well known that Sertoli cells are involved in several important processes, such as the elongation of spermatids and the formation of sperm tails ( Griswold, 2004 ), among others. Because Sertoli cell number covaries with testis mass and sperm function in red deer ( Pintus, Ros-Santaella & Garde, 2015 ), we hypothesize that Sertoli cells can also play a role in determining the intramale variation in sperm size, in agreement with the hypothesis given by Mossman et al (2013) . A high Sertoli cell number or functionality may lead to better-manufactured sperm, thus enhancing sperm function.…”

“…We found high variability in absolute testes mass among red deer males as previously described ( Martínez-Pastor et al, 2005 ; Pintus, Ros-Santaella & Garde, 2015 ). Studies in natural populations of ungulates, such as red deer and Soay sheep, have shown that testes size (both relative and absolute) is positively correlated with antler and horn size ( Preston et al, 2003 ; Malo et al, 2005a ), copula rates, and siring success ( Preston et al, 2003 ).…”

“…Because sperm competition predicts intramale variation in sperm size across related taxa (see references above), low variation in sperm size in red deer may confer an advantage in post-copulatory sexual selection by enhancing sperm competitiveness. Second, taking into account that testicular size is positively related to elaborate pre-copulatory traits (antlers, male–male competition; Malo et al, 2005a ) and shows high variability between stags ( Martínez-Pastor et al, 2005 ; Pintus, Ros-Santaella & Garde, 2015 ), we hypothesized that variation in absolute testes mass is related to the intramale variation in sperm size as demonstrated at the interspecific level in several animal taxa. Under these hypotheses, we expected to find relationships between intramale variation in sperm size and sperm function, which can reveal new insights into sexual selection processes.…”

Asymmetrical size and functionality of the pampas deer (Ozotoceros bezoarticus) testes: Right testis is bigger but left testis is more efficient in spermatogenesis

“…On the other hand, Costa et al. () and Pintus, Ros‐Santaella, and Garde () did not observe any difference in weight of both testes in the brown brocket and the red deer, respectively. Similarly, Steletta, Juyena, Ponce Salazar, Ruizc, and Gutierrez () did not observe differences in spermatogenic status in both tested in alpacas, and Formighieri Bertol, Romualdo Weiss, Ernandes Kozicki, and Machinski Rangel de Abreu () did not observe differences in testes and epididymis weight or characteristics of the sperm collected from the right or left epididymis of bulls.…”

Differentiation in body and testes weight as well as sperm quality of male roe deer from the Lublin Upland in the reproductive season

“…Procesom tym towarzyszą zmiany światła kanalików plemnikotwórczych, co uwarunkowane jest wahaniami aktywności mitotycznej i mejotycznej komórek kanalików nasieniotwórczych. Wielkość jąder oraz liczba komórek Sertoliego niejednokrotnie wykorzystywane są jako miernik procesów spermatogenezy, w aspekcie ilości i jakości plemników (3,11,14,18,19,22,24).…”