Plasticity and regeneration of gonads in the annelid Pristina leidyi.

Emily S. Sloane,Alexandra E. Bely,Eduardo E. Zattara,B. Duygu Özpolat

doi:10.1186/s13227-016-0059-1

Emily S. Sloane, Alexandra E. Bely

Open Access

https://doi.org/10.1186/s13227-016-0059-1

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Abstract

BackgroundGonads 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.ResultsWe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-016-0059-1) contains supplementary material, which is available to authorized users.

Highlights

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
Gonads regress upon starvation and regrow upon refeeding We investigated whether the gonads of P. leidyi are sensitive to feeding regime by starving and refeeding worms over several weeks and assessing gonad expression of three germline/multipotency genes, homologs of piwi, nanos, and vasa (“Methods,” Experiment 1)
We found that starvation causes a marked body-wide down-regulation of germline/multipotency gene expression and appears to cause gonad size to decrease

Summary

Introduction

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. Some animals can undergo sex reversal, involving a change in gonad structure from one gonad type (e.g., testis) to another type (e.g., ovary), a phenomenon that occurs in a number of vertebrates (e.g., fish, reptiles) and invertebrates (e.g., insects, mollusks) [10]. In groups such as colonial sea squirts, cnidarians, and sponges, gonads can form in individuals that have formed by asexual reproduction (e.g., budding) rather than by embryogenesis [3, 4, 11]. Gonad plasticity and regeneration remain largely understudied topics, despite the wide phylogenetic distribution of such phenomena and the clear developmental importance of these processes

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