Reproductive diapause influences spermatogenesis and testes’ size in the diplochronous wolf spider Allocosa senex (Lycosidae, Araneae) – A case study using a non-experimental approach

Seasonality considerably impacts on the life of organisms and leads to numerous evolutionary adaptations. Some species face seasonal changes by entering a diapause during different life stages. During adulthood, a diapause in the non-reproductive period can affect male gametogenesis as, for example, it occurs in insects. Spiders are distributed worldwide and show a variety of life cycles. However, data on spiders’ life cycles and seasonal adaptations are limited. Here, we explored the effect of reproductive diapause in a seasonal spider for the first time. We used the South American sand-dwelling spider Allocosa senex as a model as this species is diplochronous, meaning that individuals live two reproductive seasons, with juveniles and adults overwintering in burrows. It has been observed that individuals of this species reduce their metabolism during the non-reproductive season, diminishing prey consumption and locomotion to a minimum. This species is also well-known for exhibiting wandering and courting females and sedentary males. We analyzed spermatogenesis throughout the male's life cycle and described the male's reproductive system and spermiogenesis using light and transmission electron microscopy. We found that spermatogenesis in A. senex is asynchronous and continuous. However, when males face the non-reproductive season, the late spermatogenic stages and spermatozoa decline, causing an interruption but not a total arrest of this process. This seasonality is also reflected in smaller testes’ size in males from the non-reproductive season than in other periods. The mechanisms and constraints are unknown, but they could be related to the metabolic depression during this life cycle period. Since sex-role reversal apparently sets a low-intensity sperm competition scenario compared with other wolf spiders, surviving two reproductive seasons may balance mating opportunities by distributing them between both periods. Thus, the partial interruption of spermatogenesis during diapause could allow new mating encounters during the second reproductive season.