Leeches of the Genus Helobdella As Model Organisms for Evo-Devo Studies

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Leeches of the Genus Helobdella As Model Organisms for Evo-Devo Studies Theory Biosci. DOI 10.1007/s12064-015-0216-4 ORIGINALPAPER Leeches of the genus Helobdella as model organisms for Evo-Devo studies Ulrich Kutschera1 • David A. Weisblat1 Received: 19 June 2015 / Accepted: 27 October 2015 Ó Springer-Verlag Berlin Heidelberg 2015 Abstract Model organisms are important tools in modern These and other Helobdella species may be taken as Evo- biology and have been used elucidate mechanism under- Devo models of leeches, clitellate annelids, and the super- lying processes, such as development, heredity, neuronal phylum Lophotrochozoa. Here we depict/discuss the biol- signaling, and phototropism, to name but a few. In this ogy/taxonomy of these Evo-Devo systems, and the chal- context, the use of model organisms is predicated on lenges of identifying species within Helobdella. In uncovering evolutionarily conserved features of biological addition, we document that H. austinensis has been processes in the expectation that the findings will be established as a new model organism that can easily be applicable to organisms that are either inaccessible or cultivated in the laboratory. Finally, we provide an updated intractable for direct experimentation. For the most part, scheme illustrating the unique germ line/soma-differentia- particular species have been adapted as model organisms tion during early development and speculate on the because they can be easily reared and manipulated in the mechanisms of sympatric speciation in this group of laboratory. In contrast, a major goal in the field of evolu- aquatic annelids. tionary developmental biology (Evo-Devo) is to identify and elucidate the differences in developmental processes Keywords Evo-Devo Á Helobdella Á Leeches Á Model among species associated with the dramatic range of body organisms Á Germ line plans among organisms, and how these differences have emerged over time in various branches of phylogeny. At first glance then, it would appear that the concept of model Introduction organisms for Evo-Devo is oxymoronic. In fact, however, laboratory-compatible, experimentally tractable species are The British naturalist Charles Darwin (1809–1882) is well of great use for Evo-Devo, subject to the condition that the known for his zoocentric book On the Origin of Species, ensemble of models investigated should reflect the range of one of the most highly cited monographs in the history of taxonomic diversity, and for this purpose glossiphoniid biology (Darwin 1859). Less well known, however, is the leeches are useful. Four decades ago (1975), leeches of the fact that Darwin devoted much of the second half of his species-rich genus Helobdella (Lophotrochozoa; Annelida; scientific career to the study of plants (Kutschera and Clitellata; Hirudinida; Glossiphoniidae) were collected in Briggs 2009). As part of this work, Darwin introduced the Stow Lake, Golden Gate Park, San Francisco, CA (USA). grass seedling as a model organism for experimental plant research in his book The Power of Movements in Plants (Darwin 1881). His description of the phototropic bending Dedicated to the memory of Ernst Mayr (1904–2005). response in dark-grown grass coleoptiles led to the dis- covery of the plant hormone auxin, and ‘‘Darwin’s model & Ulrich Kutschera organisms’’ are still in use today (Kutschera and Niklas [email protected] 2009; Kutschera and Wang 2015). 1 Department of Molecular and Cell Biology, University of In 1904, the American geneticist Thomas Hunt Morgan California, Berkeley, CA 94720-3200, USA (1866–1945) established his ‘‘Fly-laboratory’’ at Columbia 123 Theory Biosci. University, using a common, small insect species, the fruit phylogenetic tree, and is therefore concerned at least as fly Drosophila melanogaster, as an experimental organism much with differences among taxa as with their similari- to study genetic variation. 6 years later, Morgan became ties. It has also been pointed out that the factors that lead one of the founders of the chromosomal theory of heredity, scientists to adopt certain species as ‘‘model systems’’ (e.g., which was integrated into the Neo-Darwinian theory of that small body size, rapid development, and short life cycle) time (Mayr 1942). In the history of biology Morgan was a may have correlates (canalized development, condensed prominent ‘‘anti-selectionist’’ (Morgan 1916; Mayr 1982). genomes) that renders them less representative of evolu- Importantly, however, he was also the mentor of Theodo- tionary developmental diversity than might be predicted sius Dobzhansky (1900–1975), who began to study the from their phylogenetic distribution alone (Hall 1999; genetic basis of speciation in flies of the genus Drosophila, Bolker 1995, 2014). in 1928, in Morgan’s Fly-lab. Later, Dobzhansky, together Thus, while some degree of experimental tractability is with Ernst Mayr (1904–2005), founded the Synthetic essential to elucidate developmental mechanisms for Theory of Biological Evolution (Reif et al. 2000; Kutschera comparative purposes, the field of Evo-Devo requires us to 2009, 2013; Kutschera and Niklas 2004). identify and study additional models, in particular those The establishment of the first model organisms, grass representing previously under-studied branches of the coleoptiles and fruit flies (Darwin 1881; Morgan 1916) was phylogenetic tree, and to relax our demands for ease of followed by later introductions of diverse taxa, including culture and experimental simplicity. A potential side ben- viruses and bacteria, as well as many eukaryotes (some of efit of investigating new models is the element of bio- which are shown in Fig. 1). Several models were chosen prospecting involved, i.e., the possibility that studying a because particular advantageous features outweighed the new system may reveal either ‘‘new’’ cell-biological, or difficulties in procuring and maintaining them; for example developmental processes, or provide particularly clear the giant axon and giant synapse of the squid Loligo examples (or good experimental access) to phenomena that enabled fundamental discoveries in neurophysiology, have previously been difficult to examine. despite the fact that physiologists and biophysicists work- In this article, we describe the distribution, collection, ing with Loligo generally must travel to where their subject laboratory maintenance, feeding and systematics of several can be obtained. For the most part, however, species that ‘‘lab-friendly’’ freshwater glossiphoniid leech species in emerged as models (e.g., the axolotl Ambystoma mexi- the genus Helobdella (Blanchard 1896), small clitellate canum, the nematode Caenorhabditis elegans, the frog annelids (invertebrate, segmented worms) that have Xenopus laevis, the zebrafish Danio rerio, the house mouse evolved a high degree of parental care within the super- Mus musculus, and the mustard plant Arabidopsis thaliana) phylum Lophotrochozoa (molluscs, annelids, flatworms are, like Drosophila, easy to maintain, breed and manipu- and others). Pioneering studies on the development of late in the laboratory (or green house). These models have glossiphoniid leeches were carried out in 19th century therefore been extensively studied and far more is known (reviewed in Sawyer 1986). Modern cellular and molecular about their taxonomy, development, reproduction and techniques were brought to bear on studies of leech genetics compared to other taxa (Brenner 1974; Hossfeld development beginning decades later. Since the mid 1970s, 1996; Love 2009; Rader 2004; Koornneef and Meinke multiple studies have outlined processes of cell lineage and 2010; Ankeny and Leonelli 2011; Kolb et al. 2013; Reiss cell fate decisions, segmentation, spiral cleavage, and et al. 2015). The large communities of researchers dedi- growth control in several different Helobdella species (see cated to intensively studied model organisms also provide Weisblat and Kuo 2009, 2014). Unexpectedly, the genome ‘‘economy of scale’’ so that, as new experimental resources of at least one sequenced Helobdella species is now known emerge (whole genome sequencing, gene expression to have more extensive genome rearrangements—more databases, knock-out libraries, etc.), they are first brought than almost any other bilaterian animal yet examined (Si- to bear on these models. makov et al. 2013). We discuss a recent model of germline- Notwithstanding the power of the model organism soma-differentiation that may account for this highly approach, however, the focus on just a few intensely dynamic genome. studied taxa poses a limitation for understanding how the remarkable diversity of (animal and plant) body plans has evolved through modification of developmental mecha- Materials and methods nisms, a field now called evolutionary developmental biology, or Evo-Devo (Akam 1998; Hall 1999; Jenner and The genus Helobdella comprises a group of small, flat- Wills 2007; Mueller 2007; Olsson et al. 2010). By defini- tened, proboscis-bearing freshwater leeches with one pair tion, Evo-Devo requires developmental comparisons of dorsal anterior eye-spots (order Rhynchobdellidae). The among taxa representing diverse branches of the genus is thought to have evolved in what is now South 123 Theory Biosci. Fig. 1 Model organisms that have been extensively studied by generations of biologists. Charles and Francis Darwin introduced in 1881 the etiolated grass seedling (Avena sativa, Phalaris sp.) as an experimental system for the analysis of plant growth. Other important model organisms are the Axolotl Ambystoma (1890), the house mouse Mus (1910), the fruit fly Drosophila
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