Evolution of a novel developmental trajectory: fission is distinct from regeneration in the annelid Pristina leidyi

Abstract

Understanding how novelty arises has been a major focus of evolutionary developmental biology. While the origin of new genes, gene functions, and morphological features has been studied intensely, the origin of entire developmental trajectories, such as regeneration or agametic reproduction, remains poorly understood. Agametic reproduction by fission is a novel trajectory evolved numerous times among animal phyla, including Annelida, in which it is thought to arise by co-option of regeneration. To gain insight into how a novel trajectory may evolve, we investigated a relatively recent origin of fission. We performed a detailed comparison of morphogenesis during regeneration and fission in the annelid Pristina leidyi (Clitellata, Naididae), from the onset of these trajectories to the achievement of the final morphology. We find extensive similarities between fission and regeneration morphogenesis, and, of particular note, find evidence for a synapomorphy of fission and regeneration (apparently not shared with embryogenesis) in peripheral nervous system development, providing strong support for the hypothesis that fission is derived from regeneration. We also find important differences between fission and regeneration, during development of multiple organ systems. These are manifested by temporal shifts in developmental events and by the presence of elements unique to only one process. Differences are not obviously temporally clustered at the beginning, middle, or end of development but rather occur throughout, indicating that divergence has occurred along the entire developmental course of these trajectories.

Gonad establishment during asexual reproduction in the annelid Pristina leidyi

“…Under favorable conditions, P. leidyi adds new segments continuously from a subterminal posterior growth zone and reproduces asexually by paratomic fission (Bely and Wray, 2001;Dehorne, 1916;Zattara and Bely, 2011). During paratomic fission, a new tail and a new head develop within a midbody segment, forming a region of new tissue referred to as a fission zone.…”

“…Sexual individuals are hermaphroditic and develop mature gonads in two consecutive segments, a pair of testes developing in segment 6 and a pair of ovaries developing in segment 7 (corresponding, respectively, to segments VII and VIII in classical oligochaete segment notation) (Sperber, 1948). When amputated, P. leidyi rapidly regenerates anteriorly or posteriorly, developing a new head or tail in just 4-5 days (Zattara and Bely, 2011).…”

Segment formation in Annelids: patterns, processes and evolution

“…As in post-amputation regeneration, reformation of a "tail" entails regenerating a pygidium and a functioning SAZ. Reformation of a "head" entails regenerating the prostomium and a fixed number of anterior segments (Zattara and Bely, 2011). There are thus again two different pathways for segment formation, similar to post-amputation regeneration.…”

Regeneration in spiralians: evolutionary patterns and developmental processes

“…The role in regeneration of a population of large, apparently undifferentiated cells, referred to as annelid neoblasts, that are found among a number of clitellate annelids has long been debated (Stephan-Dubois, 1954;Cornec et al, 1987) and continues to be an area of active research (Tadokoro et al, 2006;Sugio et al, 2008;Myohara, 2012;Sugio et al, 2012). The blastema ultimately differentiates into most of the missing structures, though at least some components of the regenerated nervous system appear to invade the blastema from the stump (Müller et al, 2003;Müller, 2004;Müller and Henning, 2004;Zattara and Bely, 2011).…”

“…Surgical manipulations have implicated tissue interactions between the severed body wall, nerve cord, and gut in successful regeneration (Fitzharris and Lesh, 1972). After wound-healing, cells near the wound site begin proliferating and, during both anterior and posterior regeneration, form a mass of apparently undifferentiated cells, referred to as a blastema, at the wound site (Hill, 1970;Zattara and Bely, 2011). Regarding the cellular source of the blastema and regenerated structures, several histological studies indicate that all three tissue layers proliferate near the wound site and contribute to the blastema (Clark, 1972;Cornec et al, 1987), and a recent study has shown a definitive contribution of gut endoderm to the regenerated gut (Tweeten and Reiner, 2012).…”