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 Rotifers, 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 evolution. Over the past decade dynamics. molecular and experimental work on rotifers has facilitated major progress in three lines of evolution- Keywords Rotifer 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 life. 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 invertebrates that occur in case of rotifers, we are challenged to explain the freshwater, brackish water, in moss habitats, and in soil evolution of obligate asexuality (in the bdelloids) as (Wallace et al., 2006). Rotifers are particularly fasci- mode of reproduction 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 gene 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 clade within the phylogenetic animal 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, Bdelloidea. 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 Biology, McGill University, 1205 ave. Docteur-Penfield, Montreal, QC H3A 1B1, Canada microevolution 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 phylogenetics 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 Eurotatoria (i.e., the sister group relation- sively over the past 15 years (Gomez & Snell, 1996; ship between Bdelloidea and Monogononta), 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 Acanthocephala) 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 species examined are possible Seisonidea (bisexual ectoparasites on crustaceans), 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 Brachionus 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 tree of life 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 Spiralia 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 worms, 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 (sperm, 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 Bryozoa (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. animals 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 polyploidy 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 sexual reproduction, which is investing in genome (Arkhipova & Meselson, 2000). Retrotrans- the male sex (as opposed to producing only females posons are likely sexually transmitted nuclear para- in the case of asexual reproduction). 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 meiosis 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