Morphology of the male reproductive system during post-embryonic development of the termite Silvestritermes euamignathus (Isoptera: Termitidae)

Abstract

Despite the recent research on Isoptera reproduction strategies, few studies have focused on the morphophysiology of the reproductive system in Neotropical termite species. The classic literature emphasizes the development of the female reproductive apparatus, generating a knowledge gap on the male reproductive system, including its neotenic differentiation and the evolution of the seminal vesicles. The development of the reproductive system in males of Silvestritermes euamignathus was followed from firstinstar nymphs until primary kings, with emphasis on the histology of the gonads and seminal vesicles of primary and neotenic kings from field colonies. The maturation of the reproductive system follows post-embryonic development, reaching a peak of development in primary functional kings from field colonies. The testicles are already present in first-instar nymphs and show a progressive development that is completed in primary kings, which are characterized by an enlarged size and greater sperm production. Although spermatogenesis is observed in third-instar nymphs, only in fifth-instar nymphs are spermatozoa present in the testicles and in the seminal vesicles. Spermatozoa are also present in the testicles of neotenic reproductives, derived from different nymphal instars. After the foundation of a new colony and the maturation of the king, there is a significant increase in the reproductive apparatus and the testicular lobes, which mostly occupy the whole posterior abdomen in kings from field colonies. These individuals have a minimum of seven testicular lobes that are completely separated from each other and contain rounded, aflagellated spermatozoa, which are approximately 2-3 m in diameter. Four-month old kings from laboratory colonies seem to be in a period of reproductive pause, as they display fewer sperm in the seminal vesicles. The seminal vesicles are specialized portions of the vasa deferentia that play a role in storage of spermatozoa. These structures produce a proteinaceous secretion in alates that is not observed in kings. The overall results indicate early maturation of the reproductive system in males of S. euamignathus; furthermore, the reproductive status of the different individuals might be linked to the development of the testicles and the production, storage and release of spermatozoa. The lack of a proteinaceous secretion in the seminal vesicles of kings, in comparison to alates, might be related to the maturation of the individuals after colony establishment. The development of the male reproductive system is consistent with queen physogastry, but in more discreet proportions.

A Glycoproteinaceous Secretion in the Seminal Vesicles of the Termite Coptotermes gestroi (Isoptera: Rhinotermitidae)

“…Often, non-functional individuals occur in the presence of the primary reproductives, and become functional after colony orphaning [4,32]. In Silvestritermes euamignathus, spermatogenesis already occurs in third-instar nymphs, but spermatozoa were only observed in the testicular lobes of fifth-instar nymphs [33], latter than in C. gestroi. However, third-to fifth-instar nymphs of S. euamignathus may differentiate into neotenics after two successive molts [34], and these functional nymphoid neotenics present spermatozoa in the seminal vesicles [33].…”

“…The seminal vesicles of C. gestroi are individualized organs with morphological and probably functional differentiations in their different portions (proximal and distal). According to [24], the seminal vesicles are dilations of the vasa deferentia in many insects, such as observed in the higher termites, e.g., S. euamignathus [33] and some lower termites, e.g., Cryptotermes brevis [35,36]. However, in some orthopteroid insects, the seminal vesicles are not simple expansions of the ducts, but individualized structures as observed in C. gestroi.…”

Positional Relationships among Male Reproductive Organs in Insects

“…Similarly, in Drosophila melanogaster Meigen, there was a significant reduction in the testes size after five successive matings [25]. In general, testis development is closely related to spermatogenesis [26], and testis size usually increases as spermatogenesis becomes more active [27]. However, the relationship between testis size and spermatogenesis depends on the species and developmental stage.…”

A comprehensive review on the documented characteristics of four Reticulitermes termites (Rhinotermitidae, Blattodea) of China

“…All castes of termite have male and female individuals, but only the fully mature, morphological and physiological functional sexual organs were dissected out from the main reproductive castes such as primary reproductive and secondary reproductive (Su et al, 2015;Brent et al, 2016). The queen reproductive system comprises the genital cavity, accessory gland, spermatheca, oviducts, and branched ovary (Raina et al, 2007) while in king it consists of the accessory gland, ejaculatory duct, seminal vesicle, vas deferens and testis (Laranjo et al, 2018;Vargo, 2019). The ovary is composed of multiple branched oocytes that are arranged in turn inside the ovarian tubes (Husseneder et al, 2012a).…”