Characteristics and fate of the spermatozoa of Inachus phalangium (Decapoda, Majidae): Description of novel sperm structures and evidence for an additional mechanism of sperm competition in brachyura

Abstract

Various aspects of the reproductive anatomy of the spider crab Inachus phalangium are investigated utilizing light and electron microscopy. Spermatozoal ultrastructure reveals the presence of a glycocalyx in the peripheral region of the periopercular rim, never recorded before in crustacean sperm cells. Sperm cell morphological traits such as semi-lunar acrosome shape, centrally perforate and flat operculum, and absence of a thickened ring, are shared only with Macropodia longirostris, confirming a close phylogenetic relationship of these species and their separation from the other members of the family Majidae. Spermatozoa are transferred to females inside spermatophores of different sizes, but during ejaculate transfer, larger spermatophores might be ruptured by tooth-like structures present on the ejaculatory canal of the male first gonopod, releasing free sperm cells. Such a mechanism could represent the first evidence of a second form of sperm competition in conflict with sperm displacement, the only mechanism of sperm competition known among Brachyura, enabling paternity for both dominant and smaller, non-dominant, males. In addition, we propose several hypotheses concerning the remote and proximal causes of the existence of large seminal receptacles in females of I. phalangium. Among these, genetically diverse progeny, reduction of sexual harassment and phylogenetic retention seem the most plausible, while acquisition of nutrients from seminal fluids, demonstrated in other arthropods, and suggested by previous studies, could be discarded on the basis of the presented data.

Sperm ultrastructure of the spider crab Maja brachydactyla (Decapoda: Brachyura)

“…For example, the separation between the Gecarcinucidae and Potamidae families in the Potamoidea is confirmed by the presence of a middle acrosomal layer in the sperm of the Potamidae (represented by the subfamily Potamiscinae by Klaus et al, 2009). Similarly, the differences observed between the spermatozoa of Macropodia longirostris and Inachus phalangium (Rorandelli et al, 2008) and the rest of Majoidea, including the spider crab Maja brachydactyla, support the existence of a taxonomic unit within the Inachinae, as suggested by larval studies (see discussion of Rorandelli et al, 2008).…”

“…Despite its malleability, the chromatin must also possess a minimum consistency to penetrate the oocyte without causing DNA breakage. In this regard, the chromatin close to the acrosome in I. phalangium is more electron dense (greater condensation according to Rorandelli et al, 2008) than the chromatin located in the nuclear periphery. In this case, the dense inner chromatin could better resist the mechanical traction exerted during the acrosomal eversion.…”

Reproductive system and size maturity of the paddle crab Ovalipes trimaculatus (Brachyura: Portunidae) along the Argentine coast

“…These setae could rub against the abdomen during copulation (Beninger et al, 1991). In the case of setae type 4 encountered in G2, they are similar to the "pyramid-like" setae of Maja (Neumann, 1996), the "cuspidate" setae of the maxillae and maxillipeds of Cherax quadricarinatus (von Martens, 1868) studied by Garm (2004), and the "tooth-like" setae of Inachus phalangium (Fabricius, 1775) studied by Rorandelli et al (2008). Since its fused-cuticle insertion, a mechanical function could be proposed.…”

“…The G2 is inserted inside G1 and acts as a hydraulic pump to push the seminal fluid through the ejaculatory duct (Beninger et al, 1991). The gonopod tip of O. trimaculatus has a single ending similar to the genera Chionoecetes studied by Beninger et al (1991), Maja studied by Neumann (1996), and Inachus studied by Rorandelli et al (2008).…”

Spermatogenesis of the spider crab Maja brachydactyla (Decapoda: Brachyura)

“…Therefore, obtaining the complete sequence of stages throughout spermatogenesis is a difficult task that would explain why so little information is available in brachyurans. Recent studies have revealed new features of the brachyuran spermiogenesis, such as the maturation of the spermatids in the vas deferens and seminal receptacles of the snow crab Chionoecetes opilio (Sainte-Marie and Sainte-Marie, 1999a,b) and the loss of a glycocalyx in the spermatozoa of Inachus phalangium in the seminal receptacle of the females (Rorandelli et al, 2008).…”