Plasticity and Regeneration of Gonads in the Annelid Pristina Leidyi Özpolat Et Al

EvoDevo STARVATION-REFEEDING MORPHALLAXIS new gonads in orginal new gonads in previously gonadal segments non-gonadal segments Fed worm amputation Starved worm Re-Fed worm PARATOMIC FISSION EPIMORPHOSIS new gonads in new new gonads in new segments segments amputation Plasticity and regeneration of gonads in the annelid Pristina leidyi Özpolat et al. Özpolat et al. EvoDevo (2016) 7:22 DOI 10.1186/s13227-016-0059-1 Özpolat et al. EvoDevo (2016) 7:22 DOI 10.1186/s13227-016-0059-1 EvoDevo RESEARCH Open Access Plasticity and regeneration of gonads in the annelid Pristina leidyi B. Duygu Özpolat1,2* , Emily S. Sloane1, Eduardo E. Zattara1,3 and Alexandra E. Bely1* Abstract Background: Gonads are specialized gamete-producing structures that, despite their functional importance, are generated by diverse mechanisms across groups of animals and can be among the most plastic organs of the body. Annelids, the segmented worms, are a group in which gonads have been documented to be plastic and to be able to regenerate, but little is known about what factors influence gonad development or how these structures regenerate. In this study, we aimed to identify factors that influence the presence and size of gonads and to investigate gonad regeneration in the small asexually reproducing annelid, Pristina leidyi. Results: We found that gonad presence and size in asexual adult P. leidyi are highly variable across individuals and identified several factors that influence these structures. An extrinsic factor, food availability, and two intrinsic factors, individual age and parental age, strongly influence the presence and size of gonads in P. leidyi. We also found that following head amputation in this species, gonads can develop by morphallactic regeneration in previously non- gonadal segments. We also identified a sexually mature individual from our laboratory culture that demonstrates that, although our laboratory strain reproduces only asexually, it retains the potential to become fully sexual. Conclusions: Our findings demonstrate that gonads in P. leidyi display high phenotypic plasticity and flexibility with respect to their presence, their size, and the segments in which they can form. Considering our findings along with relevant data from other species, we find that, as a group, clitellate annelids can form gonads in at least four different contexts: post-starvation refeeding, fission, morphallactic regeneration, and epimorphic regeneration. This group is thus particularly useful for investigating the mechanisms involved in gonad formation and the evolution of post- embryonic phenotypic plasticity. Keywords: Piwi, Vasa, Nanos, Gonad regeneration, Germline, Phenotypic plasticity, Starvation, Asexual reproduction, Parental effect, Annelida Background larval or juvenile development, or adult sexual matura- Gonads are specialized organs that produce gametes tion (depending on the species) [1, 2]. It is at this stage and are thus fundamentally important structures in that gonads are first established in the life cycle of the the reproductive biology of many metazoans. How- animal. This initial formation of gonads is often consid- ever, gonad development is highly variable across ered the “normal” mode of gonad formation for a spe- groups of animals and gonads can be among the most cies. However, gonad presence, size, and shape can be plastic organs of the body. Gonad development is highly plastic even after this initial gonad formation often described as occurring during a typical, specific phase, and this plasticity can be manifested at several stage of the life cycle, such as during embryogenesis, points in the life cycle of an animal [3–5]. Plasticity in gonad development is manifested in a vari- *Correspondence: [email protected]; [email protected]; ety of ways in animals. In many animal groups, gonads http://www.life.umd.edu/biology/bely/belylab/BelyLab/Home.html; can regress, regrow, change in structure, form in asexu- http://www.life.umd.edu/biology/bely/belylab/BelyLab/Home.html 1 Department of Biology, University of Maryland, College Park, MD 20742, ally produced individuals, and even regenerate. In groups USA such as insects, nematodes, ribbon worms, and mice, Full list of author information is available at the end of the article gonads have been shown to atrophy during periods of © 2016 The Author(s). This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Özpolat et al. EvoDevo (2016) 7:22 Page 3 of 15 food limitation or starvation, and to regrow when food annelids are able to regenerate gonads after amputation intake increases again [6–9]. Some animals can undergo (reviewed in [16]). For example, the polychaete Capitella sex reversal, involving a change in gonad structure from teleta (Capitellidae) can regenerate ovaries in regenerated one gonad type (e.g., testis) to another type (e.g., ovary), a posterior segments [18], and among the clitellates, Lum- phenomenon that occurs in a number of vertebrates (e.g., bricillus lineatus (Enchytraeidae), Enchytraeus japon- fish, reptiles) and invertebrates (e.g., insects, mollusks) ensis (Enchytraeidae), Criodrilus lacuum (Criodrilidae), [10]. In groups such as colonial sea squirts, cnidarians, Rhynchelmis sp. (Lumbriculidae), and Stylaria lacustris and sponges, gonads can form in individuals that have (Naididae) have been documented to regenerate gonads formed by asexual reproduction (e.g., budding) rather following either anterior and/or posterior amputation than by embryogenesis [3, 4, 11]. Finally, a number of ani- ([17, 27, 29] and works by Janda reviewed in [21]). Anne- mal groups have been shown to be capable of regenerat- lids are therefore an excellent group in which to investi- ing their gonads. For example, some fish and amphibians gate plasticity of gonads. can regenerate gonadal tissue after partial or complete Pristina leidyi Smith (1896) (Clitellata: Naididae) is removal of gonads [12–14], and some flatworms and a small, freshwater annelid that is well suited to study- annelids can regenerate gonads after amputation of ing gonad plasticity and regeneration. This species can gonad-bearing body regions [15–18]. Most of the major regenerate well and can also reproduce asexually by fis- model systems of developmental biology have none or sion. Pristina leidyi is hermaphroditic and forms gonads only a few of these properties of gonad plasticity. Conse- in two consecutive anterior segments: a pair of testes quently, gonad plasticity and regeneration remain largely in segment 6 and a pair of ovaries in segment 7 (corre- understudied topics, despite the wide phylogenetic distri- sponding, respectively, to segments VII and VIII in clas- bution of such phenomena and the clear developmental sical oligochaete segment notation, which includes the importance of these processes. asegmental prostomium in the segment count) [30]. Annelids, the segmented worms, are a group of ani- Although this species can reproduce sexually, and does mals in which several forms of gonad plasticity have so at characteristic times of year in nature [21, 31], most been described [19–21]. With respect to the location generations in the wild are asexual. The cues for initiat- of gametogenesis and the presence of gonads, annelids ing sexual reproduction are not yet known in this species, fall broadly into two groups. In non-clitellate annelids and laboratory-cultured strains reproduce only asexu- (polychaetes), which represent the bulk of annelid diver- ally. Interestingly, we have previously shown that even in sity, gametogenesis typically occurs in most segments long-term asexual laboratory cultures, asexually repro- along the body and gonads are either not present at all ducing individuals develop gonads [32]. Although these or are relatively simple in form, with only a thin perito- gonads do not develop to the large size characteristic of neum encasing the germ cells [19, 22]. In species without sexually mature individuals, their presence does indicate gonads at all, gamete-forming germ cells are simply dis- that sexual development is ongoing in asexual individu- tributed along the body, often in association with para- als. This same study also found that homologs of the ger- podia (lateral appendages), and without a peritoneum mline/multipotency genes [33] piwi, nanos, and vasa are encasing the germ cells. In clitellate annelids, a large expressed in both testes and ovaries of asexual P. leidyi, annelid subclade that includes leeches and oligochaetes, as well as in regions of active tissue development (i.e., the gonads are restricted to only a few anterior segments and regeneration blastema, posterior growth zone, and fission gametogenesis occurs within gonads, which are typically zone). Because gonads are relatively small and transpar- pear-shaped sac-like structures attached to the poste- ent in asexual individuals, gene expression thus provides rior face of a segmental septum, near the ventral nerve a useful way to identify these structures, which are other- cord [21]. In several annelids, food

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