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A place for nourishment or a slaughterhouse? Elucidating the role of spermathecae in the terrestrial annelid Hormogaster elisae (Clitellata: Opisthopora: Hormogastridae)

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A place for nourishment or a slaughterhouse? Elucidating the role of spermathecae in the terrestrial annelid Hormogaster elisae (Clitellata: Opisthopora: Hormogastridae)
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           1 3 Zoomorphology Evolutionary, Comparative andFunctional Morphology ISSN 0720-213XVolume 131Number 2 Zoomorphology (2012) 131:171-184DOI 10.1007/s00435-012-0151-6  place for nourishment or aslaughterhouse? Elucidating the roleof spermathecae in the terrestrial annelid Hormogaster elisae  (Clitellata:Opisthopora: Hormogastridae) Marta Novo, Ana Riesgo, CarmenRoldán, Gonzalo Giribet & Darío J. DíazCosín           1 3 Your article is protected by copyright andall rights are held exclusively by Springer-Verlag. This e-offprint is for personal use onlyand shall not be self-archived in electronicrepositories. If you wish to self-archive yourwork, please use the accepted author’sversion for posting to your own website oryour institution’s repository. You may furtherdeposit the accepted author’s version on afunder’s repository at a funder’s request,provided it is not made publicly available until12 months after publication.  ORIGINAL PAPER A place for nourishment or a slaughterhouse? Elucidating the roleof spermathecae in the terrestrial annelid  Hormogaster elisae (Clitellata: Opisthopora: Hormogastridae) Marta Novo  • Ana Riesgo  • Carmen Rolda´n  • Gonzalo Giribet  • Darı´o J. Dı´az Cosı´n Received: 23 November 2011/Revised: 1 February 2012/Accepted: 3 February 2012/Published online: 28 February 2012   Springer-Verlag 2012 Abstract  The capacity of storing sperm within thefemale reproductive tract occurs widely across vertebrateand invertebrate species. Although the type and position of spermathecae have been commonly used as a taxonomiccharacter in Opisthopora, few studies have focused on theultrastructural description of these interesting storageorgans. This study is the first to report on the ultrastructureof the spermathecae and spermatozoa of   Hormogaster elisae , an endemism of the central area of the IberianPeninsula that presents two pairs of tubular spermathecae.Light and electron microscopy showed that the spermath-ecae are full of highly packed spermatozoa embedded in anelectron-dense substance. Two layers constitute the sper-mathecal wall. The outer layer consists of peritoneal cells,collagenous basal laminae at different levels, several layersof striated muscle, and numerous blood vessels. The innerlayer is a monostratified epithelium of prismatic cellspresenting long and abundant microvilli probably for themaintenance of a favorable environment for the sperma-tozoa. The epithelial cells show high activity, and threedifferent types of secretions were detected: holocrine,merocrine, and apocrine, whose hypothetical function onnourishment and/or causing quiescence is discussed here.Although no phagocytotic processes were detected, somesperm cells were observed in digestive vesicles within thecytoplasm of the epithelial cells, and there was also evi-dence of active sperm entrance into the epithelium. A placefor nourishment or a slaughterhouse? Probably both. Keywords  Annelida    Opisthopora    Spermathecae   Spermatozoa    Sperm digestion    Transmission electronmicroscopy    Secretions Introduction Female sperm storage has been observed in many differentanimal groups, both vertebrates (Birkhead and Møller1993; Holt and Lloyd 2010) and invertebrates, such as Insecta (e.g., Hellriegel and Bernasconi 2000), Mollusca(e.g., Beese et al. 2009), and Annelida (e.g., Hilario et al.2005; Jamieson 2006), including Opisthopora (e.g., Jamieson 1981; Edwards and Bohlen 1996), but further studies are needed to completely understand this peculiarreproductive strategy. Sperm storage in the female bodyallows the spermatozoa to be used for fertilization sometime after mating, which is particularly useful for Opis-thopora living in the soil, because in this cryptic milieu,favorable conditions are discontinuous in time and space.Another advantage of sperm storage is that females mayinfluence paternity by extruding or digesting sperm of different males selectively (Eberhard 1985; Birkhead et al.1993) and/or by using physiological, anatomical, andfunctional adaptations of their sperm storage organs(Eberhard 1996).Although different reproductive strategies are present insoil Opistophora, including parthenogenesis, these animals Marta Novo and Ana Riesgo equally contributed to this work.Communicated by T. Bartolomaeus.M. Novo ( & )    A. Riesgo    G. GiribetDepartment of Organismic and Evolutionary Biology,Museum of Comparative Zoology, Harvard University,26 Oxford Street, Cambridge, MA 02138, USAe-mail: mnrodrig@fas.harvard.eduM. Novo    C. Rolda´n    D. J. Dı´az Cosı´nDepartamento de Zoologı´a y Antropologı´a Fı´sica,Facultad de Biologı´a, Universidad Complutense de Madrid,C/Jose´ Antonio Nova´is, 28040 Madrid, Spain  1 3 Zoomorphology (2012) 131:171–184DOI 10.1007/s00435-012-0151-6  are usually thought to be obligate out-crossing simulta-neous hermaphrodites (i.e., suing reciprocal insemination,simultaneously transferring and receiving sperm duringcopulation). At least this is the case of the best-knownspecies,  Lumbricus terrestris  Linnæus 1758 (Dı´az Cosı´net al. 2011). A similar reproductive strategy is presented by  Hormogaster elisae  A´lvarez, 1977, endogeic and endemicto the central area of the Iberian Peninsula.  Hormogaster elisae  represents a complex of cryptic species (Novo et al.2009, 2010a), which is paraphyletic relative to the remaining species in the genus (Novo et al. 2011). It has along life cycle, when compared to other terrestrial Opis-thopora species, needing, on average, 484 days for clitel-lum development from hatchling, and presents a cocoonproduction rate between 0.9 and 2.29 per specimen per year(Dı´az Cosı´n et al. 2009).As a part of the female reproductive system, terrestrialOpisthopora present spermathecae (of different shapes:tubular, spherical or flattened) of ectodermic origin(Jamieson 1992), where they store the received allosperm.Spermathecae are almost always paired organs:  Lumbricusterrestris  presents two pairs, whereas other species mayhave more, up to seven pairs in  Octodrilus complanatus (Duge`s, 1828)  ,  but some have fewer or none (Edwards andBohlen 1996). Also, 138 intersegmental sets of spermath-ecae have been exceptionally cited in  Alma  (Brinkhurst andJamieson 1971). The spermathecae are attached to the bodywall by short ducts, and many species of megascolecidspresent one or more diverticula arising from these ducts(Jamieson 2001). Moreover, some terrestrial Opisthopora,including some hormogastrid species (Qiu and Bouche´1998), present different sperm loads within a single sper-mathecae. Inside the spermathecae, sperm cells are usuallyhighly packed among an electron-dense nutritive sub-stance, although in some instances, some species such as  Megascolides australis  McCoy, 1878  ,  present a peculiarsperm grouping known as spermatozeugmata (i.e., sperm inoriented bundles, Vanpraagh 1995).  Hormogaster elisae  presents two pairs of large tubularspermathecae, usually full of sperm in mature individuals.The posterior pair of spermathecae has been found tocontain more allosperm than the anterior pair (Garvı´n et al . 2003). It presents no subdivision of the spermathecae, andno differential storage of sperm from distinct partners isperformed, as shown by Novo et al. (2010b), who could notidentify differences in the srcin of the allosperm found inthe four spermathecae of   H. elisae  using microsatellitemarkers. This may indicate that if sperm competition werepresent in these animals, it should be orchestrated bymechanisms inside each spermatheca. Besides an apparentnon-existent differential storage, another possible mecha-nism of sperm competition in terrestrial Opisthopora is oldsperm digestion, as reported in  Dendrobaena subrubicunda Eisen, 1874 and other lumbricid species by Richards andFleming (1982) or in  Amynthas  and  Metaphire  species byTeisaire and Rolda´n (1995). Long storage of sperm requires the existence of amaintenance mechanism for sperm survival. Some authorshave suggested the active contribution of the spermathecalepithelium to the successful preservation of sperm cells bysupplying nourishing substances and providing a favorableluminal environment (Grove 1925; Varuta and More 1972; Vyas and Dev 1972; Fleming 1981). Butt and Nuutinen (1998) reported that  L. terrestris  successfully maintainedthe received sperm up to six months. Meyer and Bowman(1994), even though they were not measuring cocoon via-bility, observed that  Eisenia fetida  (Savigny, 1826) pro-duced cocoons for up to 12 months after isolation. Garvı´net al. (2003) reported spermathecae full of spermatozoaduring diapause in  H. elisae , which suggests that mainte-nance processes of the sperm within the spermathecae aretaking place.Very few studies have focused on the morphology andultrastructure of the spermathecae in Opisthopora andTubificata (Fleming 1981; Jamieson 1981, 1992; Teisaire and Rolda´n 1995; Vanpraagh 1995). Here, we present a detailed description of morphological features at theultrastructural level of the spermathecae and spermatozoaof   H. elisae  for the first time using both light and trans-mission electron microscopy. Our aim was to unravel therole of the spermathecal wall in the maintenance of sperm,as well as the interactions between sperm cells and thespermathecal wall (i.e., the possible presence of spermdegradation, sperm lysis of the spermathecal wall, etc.).We found that the epithelial cells of the wall produce threedifferent types of secretions (i.e., merocrine, holocrine, andapocrine) deduced to nourish the stored sperm. Also, thefrequent observations of non-aberrant sperm within theepithelial cells suggest that these cells are actively digest-ing sperm, although phagocytosis of sperm cells was notclear in this case. In turn, it appeared that spermatozoalysed the epithelial membranes to enter the cells. Materials and methods Specimen samplingClitellate specimens of   Hormogaster elisae  were collectedby digging and hand sorting in El Molar, Madrid, Spain(GPS: N 40  44 0 22.9 00 , W 3  33 0 53.1 00 ). The climatic andedaphic characteristics of the site are fully described inValle et al .  (1997) and Gutie´rrez et al. (2006). Four spec-imens were collected every 2 months between November2007 and May 2008, in order to evaluate the differences inthe structure of the spermathecae and their contents along 172 Zoomorphology (2012) 131:171–184  1 3  Fig. 1  General structure of the spermathecae of   Hormogaster elisae using light microscopy.  a . Overall view of one spermatheca showingits wall and the lumen full of highly packed sperm.  b . Close-up of thespermathecal wall composed by two layers: outer epithelium withperitoneal cells and the inner epithelium with prismatic epithelialcells, showing the lobulated profile sometimes found due to spermintrusions.  c – e . Details of different types of secretions produced bythe epithelial cells: holocrine secretions and apocrine secretions.In this case, the spermathecal wall shows the commonly observedlinear profile although some sperm intrusions are present.  f  . Overviewof a spermatheca containing very compacted sperm and a central zonewith different affinity for the stain that could be interpreted as spermdegeneration. Abbreviations:  as  apocrine secretions,  bl  basal lamina, ec  epithelial cells,  hs  holocrine secretions,  l  lumen,  pc  peritonealcells,  sp  spermatozoa,  spd   sperm degeneration,  sw  spermathecal wallZoomorphology (2012) 131:171–184 173  1 3
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