Phylogenetic Distribution of Regeneration and Asexual Reproduction in Annelida: Regeneration Is Ancestral and fission Evolves in Regenerative Clades
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Invertebrate Biology 135(4): 400–414. © 2016 The Authors. Invertebrate Biology published by Wiley Periodicals, Inc. on behalf of American Microscopical Society. This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. DOI: 10.1111/ivb.12151 Phylogenetic distribution of regeneration and asexual reproduction in Annelida: regeneration is ancestral and fission evolves in regenerative clades Eduardo E. Zattara,1,2,3,a and Alexandra E. Bely3 1Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, District of Columbia 20560-0163, USA 2Department of Biology, Indiana University, Bloomington, Indiana 47405-7107, USA 3Department of Biology, University of Maryland, College Park, Maryland 20742, USA Abstract. Regeneration, the ability to replace lost body structures, and agametic asexual reproduction, such as fission and budding, are post-embryonic developmental capabilities widely distributed yet highly variable across animals. Regeneration capabilities vary dramat- ically both within and across phyla, but the evolution of regeneration ability has rarely been reconstructed in an explicitly phylogenetic context. Agametic reproduction appears strongly associated with high regenerative abilities, and there are also extensive developmental simi- larities between these two processes, suggesting that the two are evolutionarily related. However, the directionality leading to this relationship remains unclear: while it has been proposed that regeneration precedes asexual reproduction, the reverse hypothesis has also been put forward. Here, we use phylogenetically explicit methods to reconstruct broad pat- terns of regeneration evolution and formally test these hypotheses about the evolution of fission in the phylum Annelida (segmented worms). We compiled from the literature a large dataset of information on anterior regeneration, posterior regeneration, and fission abilities for 401 species and mapped this information onto a phylogenetic tree based on recent molecular studies. We used Markovian maximum likelihood and Bayesian MCMC methods to evaluate different models for the evolution of regeneration and fission and to estimate the likelihood of each of these traits being present at each node of the tree. Our results strongly support anterior and posterior regeneration ability being present at the basal node of the annelid tree and being lost 18 and 5 times, respectively, but never regained. By con- trast, the ability to fission is reconstructed as being absent at the basal node and being gained at least 19 times, with several possible losses. Models assuming independent evolu- tion of regeneration and fission yield significantly lower likelihoods. Our findings suggest that anterior and posterior regeneration are ancestral for Annelida and are consistent with the hypothesis that regenerative ability is required to evolve fission. Additional key words: Annelida, regeneration, asexual reproduction, fission, phylogenetic methods, evolution, post-embryonic development, ancestral state reconstruction In animals, several possible developmental trajec- are highly variable across animal phylogeny (Ghis- tories can generate the adult phenotype, including elin 1987; Adiyodi & Adiyodi 1994; Brockes & embryogenesis, regeneration, and agametic asexual Kumar 2008; Bely & Nyberg 2010), indicating that reproduction (e.g., fission, budding). While embryo- these trajectories have been evolutionarily labile. genesis is clearly a shared, ancestral feature of ani- Elucidating the pattern of evolution of regeneration mals, both regeneration and agametic reproduction and agametic reproduction can thus provide insights into how developmental trajectories evolve. aAuthor for correspondence. Although regeneration and agametic reproduction E-mail: [email protected] have distinct functions (repair and restoration in the Regeneration and fission in Annelida 401 former; reproduction in the latter) and distinct required to evolve agametic reproduction, then potential adaptive values, they have often been clades with agametic reproduction are expected to viewed as largely equivalent processes (Bourne 1891; be nested within clades that can regenerate, and Galloway 1899; Dehorne 1916; Berrill 1952; Gibson gains of agametic reproduction are expected to fall & Paterson 2003). This is because regeneration and on branches inferred to have sufficient regenerative agametic reproduction tend to co-occur across the abilities. If regeneration evolves as an exaptation animal phylogeny (Vorontsova & Liosner 1960; of agametic reproduction, then regenerating clades Hughes 1989), with organisms that are capable of should nest within clades with agametic reproduc- agametic reproduction typically having high regener- tion, and gains of regeneration are expected to fall ative abilities, and because the developmental on branches inferred to have agametic reproduc- processes underlying these two trajectories within a tion. These two hypotheses, along with the null given organism tend to be extremely similar hypothesis that regeneration and agametic repro- (Adiyodi & Adiyodi 1994; Rinkevich & Matranga duction evolve independently of each other, can 2009; Zattara & Bely 2011). Recent studies demon- be tested by mapping regeneration and fission strate, however, that these developmental trajecto- abilities onto a phylogenetic tree and reconstruct- ries can be decoupled (Bely 1999a; Brockes & ing ancestral states (Pagel et al. 2004; Paradis Kumar 2008; Bely & Sikes 2010) and that, although 2011). very similar, they are not developmentally equiva- The phylum Annelida, the segmented worms, is a lent: differences are evident in the extent and timing group that is particularly well suited for investigat- of tissue remodeling as well as gene expression (Hori ing the evolutionary patterns of regeneration and & Kishida 1998, 2001; Bely & Wray 2001; Martinez agametic reproduction. The relatively uniform body et al. 2005; Reitzel et al. 2007; Burton & Finnerty plan of annelids (Fig. 1A) facilitates comparisons 2009; Lengfeld et al. 2009; Zattara & Bely 2011). of regenerative potential and fission modes, and Thus, regeneration and agametic reproduction variation in both regenerative and fission abilities is appear to be evolutionarily related but not equiva- well documented in the phylum (Bely 1999b, 2006, lent trajectories. 2010; Zattara 2012; Bely et al. 2014). Following But which trajectory evolves first, and which fol- transverse amputation of the body, species vary in lows, remains debated. The most widely held view is their ability to regenerate anterior structures from that regenerative capabilities are a pre-requisite for an anterior wound surface (anterior regeneration) the evolution of agametic reproduction (Morgan as well as their ability to regenerate posterior struc- 1901; Vorontsova & Liosner 1960; Schroeder & tures from a posterior wound surface (posterior Hermans 1975; Ghiselin 1987), and thus that regeneration) (Fig. 1B). Although rare overall in regeneration evolves first. However, it has also been the phylum, agametic reproduction by fission proposed that regeneration evolves as an epiphe- occurs in many groups of annelids (Schroeder & nomenon of agametic reproduction (Darwin 1868; Hermans 1975). Two main types of fission have Sanchez Alvarado 2000; Giangrande & Licciano been described (Fig. 1C): architomy (also known as 2014), and thus that agametic reproduction evolves fragmentation or scissiparity), in which physical first. Arguments in support of the “regeneration separation precedes the development of new tissues; first” hypothesis are based mostly on the phyloge- and paratomy, in which new tissues develop prior netic distribution of these trajectories, with regenera- to physical separation. Much progress has recently tion having a much broader distribution than does been made in clarifying deep level relationships agametic reproduction, and the suggestion that the among major annelid clades (Struck et al. 2011; evolution of agametic reproduction would seem to Weigert et al. 2014; Andrade et al. 2015; Weigert & require a pre-existing ability to regrow the relevant Bleidorn 2016), providing enough phylogenetic con- body parts. Arguments in support of the “agametic text for interpreting variation in regeneration and reproduction first” hypothesis are typically based on fission. the prevalence of agametic reproduction among In this study, we generate the first phylum-wide, basal animals, suggesting it could be ancestral for species-specific mapping of presence/absence of animals, and on the expectation that high regenera- regeneration and fission ability. We estimate ances- tion ability would be an exaptation of an organism’s tral character states for nodes within the annelid ability to reproduce agametically. tree, allowing us to infer the most likely capabilities These two scenarios make different predictions for the last common ancestor of Annelida, and test regarding the expected phylogenetic patterns of hypotheses regarding the evolutionary relationship these two trajectories. If regenerative ability is between regeneration and fission. Invertebrate Biology vol. 135, no. 4, December 2016 402 Zattara & Bely A prostomium pygidium (asegmental) segments (asegmental) anterior posterior growth zone growth zone B anterior posterior C agametic