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Home , Acanthocephala, Adinetidae, Bdelloidea, Brachionus calyciflorus, Rotaria, Rotifer

Hydrobiologia (2011) 662:11–18 DOI 10.1007/s10750-010-0515-1

ROTIFERA XII

Rotifers: excellent subjects for the study of macro- and microevolutionary change

Gregor F. Fussmann

Published online: 1 November 2010 Ó Springer Science+Business Media B.V. 2010

Abstract , both as individuals and as a nature. These features make them excellent eukaryotic phylogenetic group, are particularly worthwhile sub- model systems for the study of eco-evolutionary jects for the study of . Over the past decade dynamics. molecular and experimental work on rotifers has facilitated major progress in three lines of evolution- Keywords phylogeny Á Asexuality Á ary research. First, we continue to reveal the phy- Eco-evolutionary dynamics logentic relationships within the taxon Rotifera and its placement within the tree of . Second, we have gained a better understanding of how macroevolu- Introduction tionary transitions occur and how evolutionary strat- egies can be maintained over millions of years. In the Rotifers are microscopic that occur in case of rotifers, we are challenged to explain the freshwater, brackish water, in habitats, and in soil evolution of obligate asexuality (in the bdelloids) as (Wallace et al., 2006). Rotifers are particularly fasci- mode of and how speciation occurs in nating and suitable objects for the study of evolution the absence of sex. Recent research with bdelloid roti- and, over the past decade, featured prominently in fers has identified novel mechanisms such as horizon- research on both macro- and microevolutionary tal transfer and resistance to radiation as factors change. I, here, review the recent developments in potentially affecting macroevolutionary change. Third, three fields of research on rotifer evolution. First, we are finding that microevolutionary change can be I report on the state of the art in the phylogeny of the sufficiently rapid to interact with ecological dynamics. Rotifera: the proposed (and still contentious) phylo- Rotifers can be easily cultured, reproduce quickly, and genetic evolution within the Rotifera and the place- occur at high levels of clonal, genetic diversity in ment of this within the phylogenetic tree. Second, I describe a body of research that is concerned with the apparent asexuality of the rotifer taxon Guest editors: N. Walz, R. Adrian, J.J. Gilbert, . Are the bdelloids truly ancient asexuals, M.T. Monaghan, G. Weithoff & H. Zimmermann-Timm / Rotifera XII: New aspects in rotifer evolution, genetics, if so, how did they evolve without sex, and how is reproduction, ecology and biogeography speciation possible in such a taxon? Finally, I summa- rize the findings of a line of research that employs fast- & G. F. Fussmann ( ) growing, clonal rotifers for the study of experimental Department of , McGill University, 1205 ave. Docteur-Penfield, Montreal, QC H3A 1B1, Canada that can happen at the time scale of e-mail: [email protected] ecological dynamics (‘‘eco-evolutionary dynamics’’, 123 12 Hydrobiologia (2011) 662:11–18

Fussmann et al. (2007)). In each case, the special group relationship between acanthocephalans and biology of rotifers motivated the research (and the use Bdelloidea. More recent studies that used broader of rotifers) but the results inform general principles of genetic data bases came to the same conclusion and evolution. (Garcia-Varela & Nadler, 2006; Witek et al., 2008). ‘‘Cryptic speciation’’ of populations (e.g., major However, other studies based on molecular or on a genetic divergence of regionally distributed populations combination of molecular and morphological evi- without morphological diversification) is another evo- dence proposed different phylogenies. Mark Welch lutionary dynamic that is wide-spread among rotifers (2000) and Herlyn et al. (2003) both retained the and has been investigated thoroughly and exten- traditional (i.e., the sister group relation- sively over the past 15 years (Gomez & Snell, 1996; ship between Bdelloidea and ), the Gomez et al., 2002; Derry et al., 2003; Fontaneto et al., latter as a sister taxon of the acanthocephalans, the 2008; Fontaneto et al., 2011). Gomez (2005)reviewed former as a sister taxon of a group joining acantho- this research recently, and it is therefore omitted here. cephalans and seisonids. Another alternative is the existence of a group Hemirotifera (Bdelloidea, Sei- sonidea and ) as sister taxon of the Phylogeny of Rotifera monogononts (Sørensen & Giribet, 2006). The use of different molecular loci and differences in the Traditionally, the Rotifera comprised the three taxa number and identity of examined are possible Seisonidea (bisexual ectoparasites on ), reasons for the vastly differing rotifer phylogenies Monogononta (cyclical parthenogens with haploid that these and other authors proposed. For instance, dwarf males) and Bdelloidea (supposedly an asexual, some phylogenies are based on plicatilis all-female clade). Further, a sister group relationship as a sole member of the monogononts or lack between bdelloids and monogononts as Eurotatoria material from the Seisonidea altogether. was supported by a number of morphological charac- The placement of the rotifers (or better: the ters (Melone et al., 1998) and suggested an evolu- Syndermata) within the animal is also a tionary trend toward the loss of sexuality culminating contentious matter and subject of current, molecular- in its complete abandonment in the bdelloids. With based research. As a consensus the placement of the arrival of DNA-based techniques, this view of Syndermata within the seems to emerge, rotifer phylogeny has been amended and revised. based on morphology and 16S/18S rRNA (Garey First, a close relationship of the Acanthocephala, a et al., 1996; Garey et al., 1998) and, more recently, taxon of endoparasitic , and the Rotifera was based on ‘‘expressed sequence tags’’ (ESTs) from revealed. The name Syndermata, originally proposed ribosomal proteins (Witek et al., 2008; Witek et al., by Ahlrichs (1995) based on morphological characters 2009). Syndermata are likely to form a taxon together (, intracytoplasmic lamina), is now widely with the Gnathostomulida (Garey et al., 1998; Witek accepted for a taxon uniting acanthocephalans, seiso- et al., 2009) that is either directly a sister group of the nids, monogononts, and bdelloids (Funch et al., 2005). Platyhelminthes (Garey et al., 1998) or related to a Second, the phylogenetic relationship among these clade comprising Platyhelminthes, Annelida, Mol- four groups is far from being resolved and is the object lusca and (Witek et al., 2008). of intensive ongoing research, using increasingly The following two sections are concerned with refined molecular and character-based data bases. lines of research that use rotifers as model organisms Critically, many phylogenies no longer postulate a to investigate the mechanism underlying evolutionary sister group relationship between the acanthocepha- change and stasis. lans and the three traditional rotifer groups, which essentially would mean that the taxon Rotifera is paraphyletic and the name Rotifera should not be used Ancient asexuality of bdelloid rotifers unless it includes the Acanthocephala (i.e., synony- mously with Syndermata). The evolution and maintenance of sexuality among Based on 18S rRNA gene sequences, Garey et al. is a topic that has fascinated generations of (1996) provided early molecular evidence for a sister evolutionary biologists. Several potential advantages 123 Hydrobiologia (2011) 662:11–18 13 of sex—as opposed to its alternative, asexual repro- However, several studies show that the origin of duction—have been put forward: sex entails the dates back a very long time ago (Mark recombination of genetic material, and thus enables Welch et al., 2004a; Mark Welch et al., 2008). Very populations to rapidly adapt to environmental recently, Hur et al. (2009) found that tetraploidy in change; sex leads to the quick spreading of benefi- two bdelloid families was established before these cial and/or the purging of deleterious mutations families diverged and probably also before the (Bell, 1982). Given how widespread sexual reproduc- bdelloid radiation in general. Taken together, these tion is among animals, it is generally assumed that sex studies provide strong evidence of ancient bdelloid is an evolutionarily successful strategy and that its asexuality. This evidence is complemented by the potential advantages must outweigh the major disad- apparent scarcity of retrotransposons in the bdelloid vantage of , which is investing in (Arkhipova & Meselson, 2000). Retrotrans- the male sex (as opposed to producing only females posons are likely sexually transmitted nuclear para- in the case of ). In this context, it sites; at the same time, one of the advantages of sex is puzzling that, with the bdelloid rotifers, a whole may consist in limiting the deleterious effects result- clade of animals exists for which males, hermaphro- ing from retrotransposon insertions (Arkhipova & dites and are unknown. Because such a group Meselson, 2000; Arkhipova & Meselson, 2005). It of animals is normally expected to have a short appears that bdelloids have found a way to avoid the evolutionary life span the absence of sex in the deleterious load associated with this of trans- bdelloids has been dubbed an ‘‘evolutionary scandal’’ posons. The genome of bdelloids was initially (Maynard Smith, 1986). Over the past decade, bdel- believed to be entirely free of retrotransposons loids have been the object of intensive research aimed (Arkhipova & Meselson, 2000) but recently low at understanding how a group of organisms can copy numbers of special (LTR type) retrotransposons survive, evolve and speciate over millions of years were detected that possibly originate from an exog- without sexual reproduction. enous source (Gladyshev et al., 2007). Fossil records show that, as a clade, bdelloids are If we take for granted that bdelloids as a clade at least 35 million years old (Poinar & Ricci, 1992; have forgone sexual reproduction for many millions Waggoner & Poinar, 1993). However, ‘‘absence of of years the question arises how they cope with the evidence does not equal evidence for absence’’ supposed disadvantages of having no sex. Research (Schurko et al., 2009). What is the evidence that addressing this question has focused on the increased bdelloids did not have (even occasional or cryptic) deleterious mutation load that is expected to accu- sex over this enormous period? In diploid asexual mulate in the absence of sex and recombination. The lineages, the two alleles of a gene are expected to negative effect on fitness of mutation load accumu- accumulate different mutations over time and grad- lating in the absence of sex has recently been ually become more different in sequence (Birky, demonstrated in experimental populations of the 2004). In a groundbreaking paper, Mark Welch & Caenorhabditis elegans that were reared Meselson (2000) demonstrated exactly this allelic over many generations under conditions of either sequence divergence in four species of bdelloid obligate self-fertilization or outcrossing (Morran rotifers. Sequence divergence was vastly higher et al., 2009). If bdelloid rotifers indeed never engage between alleles of several bdelloid than in outcrossing, two strategies are conceivable: bdel- between copies of the same genes in sexually loids are resistant, i.e., they do not incur increased reproducing monogonont rotifers. A follow-up study deleterious mutation load in the first place; or (Mark Welch et al., 2004b) ruled out that bdelloid bdelloids are tolerant, i.e., they do face mutation alleles are so similar that they cannot be distinguished load but have evolved measures that protect them from one another, as would happen if the bdelloid from the negative consequences. There is good genome were the result of relatively recent duplica- evidence that bdelloids do indeed face the adverse tion events. As a caveat, the divergent gene copies effects of increased mutations. First, bdelloids encoun- in bdelloids are indeed very likely a result of degen- ter roughly the same synonymous nucleotide substitu- erate ancient tetraploidy, which potentially indi- tion rates as monogononts in the gene hsp82 (coding cates hybridization of bdelloid species in the past. for a heat shock protein), i.e., they are not capable of 123 14 Hydrobiologia (2011) 662:11–18 limiting the frequency with which they are hit by movement of genes from other organisms to bdel- mutations (Mark Welch & Meselson, 2001). Second, loids by means other than direct descent. Surpris- bdelloids also accumulate higher frequencies of ingly, Gladyshev et al. (2008) found that a telomeric mutations than monogononts in the mitochondrial region of the genome of the bdelloid vaga cox1 gene (Barraclough et al., 2007; but see also: contains protein-coding sequences of non-bdelloid Swanstrom et al., 2011). These mutations generate (fungal, bacterial and ) origin and that these putatively deleterious amino acid polymorphisms, sequences are transcribed and properly spliced in which means that bdelloids do experience the Adineta. These exciting findings mean that bdelloids predicted negative effects of prolonged asexuality. potentially supplement their genome with exogenous Consequently, bdelloids must have evolved adap- genes of functional importance, thereby compensat- tive responses that allow them to tolerate or com- ing for the disadvantages of asexual reproduction. pensate the effects of deleterious mutations. In the Although not proved yet, the findings also suggest past few years, several studies have identified that bdelloids should be able to horizontally molecular structures and mechanisms in bdelloids exchange genetic material among other bdelloids that can be interpreted as compensatory against or conspecifics. This would mean that bdelloids mutational load. Bdelloids show extreme resistance have developed a mechanism to exchange genes that against ionizing radiation, maintaining higher fertility has similar effects as sexual reproduction but does rates at a given dose than any other metazoan tested not involve meiosis. (Gladyshev & Meselson, 2008). This resistance is A final puzzle arising from the asexuality of likely due to a very effective DNA breakage repair bdelloids is how the group was able to evolve mechanism, and it has been suggested that bdelloids species or, better, species-like subgroups that resem- retain colinear chromosome pairs, a remnant of ble in their degree of diversification and relatedness degenerate ancient tetraploidy, as templates for the the species in sexual taxa. Barraclough et al. (2003) repair of DNA double-strand breaks (Mark Welch used genealogical theory to show that, in general, et al., 2008). In addition, it was found that bdelloids asexuals are expected to diversify into discrete can effectively take advantage of beneficial muta- genotypic and phenotypic clusters provided they tions by evolving functional divergence of former exist as a phylogenetic group for sufficiently long alleles whose sequence homogeneity is no longer periods of time. This finding has circumstantial maintained by recombination (Pouchkina-Stantcheva support from generations of rotiferologists who have et al., 2007). described hundreds of asexual bdelloid ‘‘species.’’ In A very recent study interprets the puzzling evolu- a more formal approach, Fontaneto et al. (2007) tionary persistence of asexual bdelloids from a were able to demonstrate that the genetic and different angle. Wilson & Sherman (2010) showed morphological differences among eight morpho- experimentally that populations of the bdelloid rotifer species of the bdelloid indeed show elusa can effectively eliminate specific the signature of adaptive divergence and display fungal infections by undergoing anhydrobiosis in the clustering patterns that are significantly different form of completely desiccated ‘‘tuns’’, a resting stage from those expected under neutral divergence. In characteristic of bdelloids. This finding is in line with conclusion, speciation defined as cluster-forming the which posits that sexuality morphological and ecological diversification has is advantageous because it enables hosts to deal with apparently happened in the bdelloids. It seems likely the selective pressures imposed by their coevolving that the evolution of functional divergence of former parasites. With anhydrobiosis, bdelloids appear to alleles (Pouchkina-Stantcheva et al., 2007) would have developed an alternative mechanism that allows have facilitated this macroevolutionary process. them to rid themselves from lethal parasites and Future research needs to show whether bdelloid spe- potentially makes up for the fitness-reducing effects ciation occurred under strict asexuality over millions of asexuality. of years or whether preferential horizontal gene Probably the most momentous recent discovery is transfer (Gladyshev et al., 2008) among more that massive horizontal gene transfer occurs in closely related organisms played a significant role bdelloid rotifers (Gladyshev et al., 2008), i.e., the in the process. 123 Hydrobiologia (2011) 662:11–18 15

Rapid, eco-evolutionary dynamics evidence that they themselves were the object of evolutionary change. In another dynamics Rotifers have also played an eminent role as model experiment with B. calyciflorus Fussmann et al. organisms in a line of research that investigates rapid (2003) showed that the predator in the algal-rotifer microevolutionary change and its interaction with predator–prey system can also evolve. In chemostats, ecological dynamics. The premise is that evolution- the rotifer population entirely lost its propensity to ary change can be substantial and influential over just produce sexually so that only amictic, parthenoge- a few generations and, therefore, happens at ecolog- netic reproduction occurred after several hundred ically relevant time scales (Thompson, 1998; days. This evolutionary change occurred so rapidly Fussmann et al., 2007). Planktonic monogonont that it directly interfered with the population dynam- rotifers are uniquely suitable metazoans for the study ics of B. calyciflorus. A mathematical model pre- of experimental eco-evolutionary dynamics, due to dicted that the peculiar dynamics observed in their rapid, mostly parthenogenetic reproduction replicate trials could only be explained if selection (Bennett & Boraas, 1989), because they provide against sexual reproduction was a part of the eco- genetic diversity—the raw material for evolution— evolutionary equations (Fussmann et al., 2003). conveniently packaged as separate clones and More experiments and theoretical studies are because they can be cultured in the laboratory as under way that involve rotifers as model organisms members of model ecological communities. for rapid evolutionary change in ecological commu- Chemostat populations of the monogonont rotifer nities. For instance, our group currently investigates Brachionus calyciflorus were used as predators of how rapid changes in the clumping propensity of in a series of experimental studies phytoplankton in response to rotifer grazing affect which demonstrated that prey evolution can crucially community dynamics and how model dynamics influence the dynamics of predator–prey communi- change when multiple clones of prey and predator ties. In one example, evolution led to a particular type interact with one another (Jones et al., 2009). The of elongated and out-of-phase predator–prey cycles formation of algal clumps is an evolving trait that that could be explained by the cyclical selection of is visible to the , quantifiable in experiments and phytoplankton clones (Yoshida et al., 2003) that were reduces the ability of predators to reduce their prey. either relatively defended or undefended against Mathematical models show that the dynamical by the rotifer predator (Yoshida et al., stability of rotifer-algal predator–prey systems criti- 2004). Consequently, experimental time series dis- cally depends on the effectiveness of clumping as a played such ‘‘eco-evolutionary’’ cycles only when the defense against (Jones et al., 2009; Becks genetic diversity of the phytoplankton and, hence, the et al., 2010): weak defense leads to steady state potential for evolutionary dynamics was high (i.e., dynamics, very effective defense to evolutionary multiple clones were present); communities with cycles, as those observed in Yoshida et al. (2003). monoclonal phytoplankton cultures showed the ‘‘nor- This prediction was shown to be correct in chemostat mal’’, fast cycles predicted by classical predator–prey experiments with B. calyciflorus and the clumping theory (Yoshida et al., 2003). In another experiment algae Chlamydomonas reinhardtii. The experimental with the same predator–prey system cycling was only system settled to a steady state with moderately observable in the rotifer population. The associated defended prey. However, when Chlamydomonas had cycles of the phytoplankton resource population were been exposed to predation for several months prior to effectively eliminated through compensatory evolu- the experiment, the algal prey developed far more tionary changes in the frequencies of prey genotypes effective defense. In agreement with the mathemat- that differed in their vulnerability to the rotifers ical model, the use of these pre-conditioned algae (‘‘cryptic cycles’’, Jones & Ellner, 2007; Yoshida caused a shift of the dynamics to eco-evolutionary et al., 2007). predator–prey cycles (Becks et al., 2010). In these examples, rotifers were an integral part of In this article, I reviewed the important advances the eco-evolutionary dynamics and provided the that we have made over the past decade in the selective pressure on the phytoplankton population phylogeny of rotifers, in the evolution of asexuality in that led to microevolutionary change, but there is no the bdelloids, and in eco-evolutionary dynamics 123 16 Hydrobiologia (2011) 662:11–18 involving rotifers as model organisms. The review Arkhipova, I. & M. Meselson, 2000. Transposable elements in also showed that the evolution of rotifers and sexual and ancient asexual taxa. Proceedings of the National Academy of Sciences of the United States of evolutionary research involving rotifers are active America 97: 14473–14477. fields of research that address problems of general Arkhipova, I. & M. Meselson, 2005. Deleterious transposable evolutionary relevance and, as any good science, elements and the extinction of asexuals. Bioessays 27: generate new questions as others are solved. It has 76–85. Barraclough, T. G., C. W. Birky & A. Burt, 2003. Diversifi- become clear that the phylogeny of rotifers and their cation in sexual and asexual organisms. Evolution 57: position in the tree of life is far from being resolved 2166–2172. and I foresee continuing research activity in this field Barraclough, T. G., D. Fontaneto, C. Ricci & E. A. Herniou, over the next years. The detection of horizontal gene 2007. Evidence for inefficient selection against deleteri- ous mutations in cytochrome oxidase I of asexual bdelloid transfer (Gladyshev et al., 2008) in the bdelloids put a rotifers. Molecular Biology and Evolution 24: 1952–1962. major question mark on their ancient asexuality as a Becks, L., S. P. Ellner, L. E. Jones & N. G. Hairston, 2010. group. 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