Abstract
The naked mole-rat (NMR) queen controls reproduction in her eusocial colony by usually selecting one male for reproduction and suppressing gametogenesis in all other males and females. Simplified, polymorphic and slow-swimming spermatozoa in the NMR seem to have been shaped by a low risk of sperm competition. We hypothesize that this unique mammalian social organization has had a dramatic influence on testicular features and spermatogenesis in the NMR. The testicular structure as well as spermatogenic cell types and its organization in breeding, subordinate and disperser males were studied using light microscopy and transmission electron microscopy. Even though the basic testicular design in NMRs is similar to most Afrotheria as well as some rodents with intra-abdominal testes, the Sertoli and spermatogenic cells have many atypical mammalian features. Seminiferous tubules are distended and contain large volumes of fluid while interstitial tissue cover about 50% of the testicular surface area and is mainly composed of Leydig cells. The Sertoli cell cytoplasm contains an extensive network of membranes and a variety of fluid-containing vesicles. Furthermore, Sertoli cells form numerous phagosomes that often appear as extensive accumulations of myelin. Another unusual feature of mature NMR Sertoli cells is mitotic division. While the main types of spermatogonia and spermatocytes are clearly identifiable, these cells are poorly organized and many spermatids without typical intercellular bridges are present. Spermatid heads appear to be malformed with disorganized chromatin, nuclear fragmentation and an ill-defined acrosome formed from star-like Golgi bodies. Rudimentary manchette development corresponds with the occurrence of abnormal sperm morphology. We also hypothesize that NMR testicular organization and spermiation are modified to produce spermatozoa on demand in a short period of time and subsequently use a Sertoli cell “pump” to flush the spermatozoa into short tubuli recti and simplified rete testis. Despite the difficulty in finding cellular associations during spermatogenesis, six spermatogenic stages could be described in the NMR. These numerous atypical and often simplified features of the NMR further supports the notion of degenerative orthogenesis that was selected for due to the absence of sperm competition.
Highlights
Naked mole-rats (NMRs, Heterocephalus glaber) represent one of only two eusocial mammals (Jarvis, 1981, 1985; Faulkes et al, 1991; O’Riain et al, 2000) with reproduction typically restricted to a single female and 1–3 males within large colonies varying from 40 to 90 individuals
The Leydig cells are arranged in groups of three or more cells per island and each island is contained within a layer(s) of loose connective tissue (Figures 1B,C)
While the above discussion represents a totally new explanation of the mechanism for the release of spermatozoa from the Sertoli cell it still poses the question of how does this degenerative system relates to fertility, as in all the examples we studied the breeders were proven fathers? In our previous papers we have shown the relationship between sperm degenerate features and fertility and lack of sperm competition
Summary
Naked mole-rats (NMRs, Heterocephalus glaber) represent one of only two eusocial mammals (Jarvis, 1981, 1985; Faulkes et al, 1991; O’Riain et al, 2000) with reproduction typically restricted to a single female (queen) and 1–3 males within large colonies varying from 40 to 90 individuals. Multiple-paternity has been recorded for this species (Faulkes et al, 1997), but usually the queen selects a male for life and most other males and all other females (subordinates) are reproductively suppressed (Faulkes and Abbott, 1991; Faulkes et al, 1991) This restriction of breeding to a small subset of the population presents a low risk for sperm competition and it is assumed to have shaped the sperm structure (simple and low percentage of normal forms) and motility (slow) in this species (van der Horst et al, 2011). Seasonality, reproductive lifespan, mode of fertilization and sperm competition are all factors that could influence the organization of spermatogenesis within the testis (Ramm et al, 2014)
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