Introduction

As discussed in Chapter 4, the mixed distribution of non-metameric, metameric, and segmented body plans across what molecular phylogenetics defines as the three superphyla of bilaterally symmetric animals (Deuterostomia, Ecdysozoa, Lophotrochozoa/Spiralia) evidences a much greater degree of evolutionary plasticity in developmental processes than was thought to be the case when phylogenetic trees were constructed using morphological comparisons, as exemplified in the Articulata hypothesis. To more fully understand the evident evolutionary plasticity of developmental pathways leading to the gain or loss of segmentation and metamerism, it is necessary to compare axial growth and patterning among diverse models, including both segmented and unsegmented taxa representing different branches of the phylogenetic tree.

In the 1960s and 1970s, the nervous system of the medicinal leech Hirudo emerged as a powerful system in which to study how nervous systems function at the level of individually identified cells. This work was initiated by Stephen Kuffler and John Nicholls (Kuffler and Potter 1964; Nicholls and Baylor 1968), building on Retzius’ neuroanatomical descriptions from the 19th century, and was greatly expanded by John Nicholls, Gunther Stent, and their many disciples (Muller et al. 1981). Modern studies of leech development stem largely from the decision by Gunther Stent in the mid-1970s to use these animals as models for studying neural development of leeches. He was guided in this decision contemporaneously by Roy Sawyer (Sawyer 1986; Weisblat et al. 1978) and Juan Fernandez (Fernandez and Stent 1980), and also by Whitman’s pioneering 19th century work on embryonic cell lineages (1878, 1887). In the decades since Stent’s decision, Helobdella has become among the best known models for studying spiralian development; in this chapter, we summarize our current understanding of just one aspect of Helobdella development, i.e., segmentation.

In this chapter, we present glossiphoniid leeches, more specifically species from the genus Helobdella, as useful models for studying segmentation among annelids, within the relatively understudied superphylum Lophotrochozoa/Spiralia. Breeding populations of H. austinensis (Kutschera et al. 2013), the most commonly used species at this point, are readily maintained in lab culture and produce year-round supplies of relatively large and hardy embryos that undergo stereotyped and unequal cleavages. Thus, as will be described in detail later, the early embryo contains large individually identified, experimentally accessible, lineage-restricted stem cells from which segmental mesoderm and ectoderm arise in anteroposterior progression (Weisblat and Kuo 2009, 2014). In contrast, the midgut, which also exhibits meta- meric organization, arises in parallel from a complex merger of multiple embryonic lineages and involves the initial formation and later cellularization of a syncytial yolk cell (SYC).

In addition to their experimental tractability, leeches are of interest because genomic and phylogenetic analyses of recent years have highlighted them as a group whose genome is dramatically more extensively rearranged than almost any other known animal group, relative to that inferred for the bilaterian ancestor, as judged by the loss of macrosynteny (Simakov et al. 2013). If evo-devo has a central dogma, it is that genomic changes give rise to changes in developmental mechanisms and processes, and that changes in development underlie evolutionary changes in phenotype (e.g., morphology). Thus, we can envision species evolving by proceeding stochastically through a very highly dimensional “evo-devo space” made up of all the possible combinations of genome, development, and phenotype. For each species, its evolutionary trajectory through evo-devo space is a constrained random walk, in which each step is subject to the constraints that the species remain reproductively viable at each step, and that there are different probabilities associated with different types of genomic change.

From this, it would follow that increasing the range of possible changes that are “allowed” for the evolving genome in leeches and their allies would increase their ability to explore the surrounding evo-devo space. Thus, while much of evo-devo research is essentially retrospective, for instance, comparing segmentation mechanisms across taxa with the goal of understanding how segmentation proceeded in the last common segmented ancestor at each point where this feature originated, leeches may help us to expand our appreciation of the range of possible developmental mechanisms consistent with a segmented body plan.

Traditionally, the phylum Annelida was thought to comprise three classes of (exclusively) segmented worms: polychaetes, oligochaetes, and leeches. Molecular phylogenies reveal that polychaetes are paraphyletic with respect to clitellates (comprising oligochaetes, leeches, and their allies), and that oligochaetes are paraphyletic with respect to leeches. In addition, the phylum Annelida now includes unsegmented taxa that were previously classified as separate phyla (McHugh 1997; Struck et al. 2007, 2011). This chapter summarizes the cellular processes involved in leech segmentation, which appears to be representative of the process in clitellate annelids, a monophyletic group comprising the oligochaetes and euhirudinids (the true leeches), plus two transitional groups, acanthobdellids and branchiobdellids.

 
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