PRIMER SERIES PRIMER 2643 Development 139, 2643-2653 (2012) doi:10.1242/dev.074724 © 2012. Published by The Company of Biologists Ltd Evolutionary crossroads in developmental biology: annelids David E. K. Ferrier* Summary whole to allow more robust comparisons with other phyla, as well Annelids (the segmented worms) have a long history in studies as for understanding the evolution of diversity. Much of annelid of animal developmental biology, particularly with regards to evolutionary developmental biology research, although by no their cleavage patterns during early development and their means all of it, has tended to concentrate on three particular taxa: neurobiology. With the relatively recent reorganisation of the the polychaete (see Glossary, Box 1) Platynereis dumerilii; the phylogeny of the animal kingdom, and the distinction of the polychaete Capitella teleta (previously known as Capitella sp.); super-phyla Ecdysozoa and Lophotrochozoa, an extra stimulus and the oligochaete (see Glossary, Box 1) leeches, such as for studying this phylum has arisen. As one of the major phyla Helobdella. Even within this small selection of annelids, a good within Lophotrochozoa, Annelida are playing an important role range of the diversity in annelid biology is evident. Both in deducing the developmental biology of the last common polychaetes are marine, whereas Helobdella is a freshwater ancestor of the protostomes and deuterostomes, an animal from inhabitant. The polychaetes P. dumerilii and C. teleta are indirect which >98% of all described animal species evolved. developers (see Glossary, Box 1), with a larval stage followed by metamorphosis into the adult form, whereas Helobdella is a direct Key words: Annelida, Polychaetes, Segmentation, Regeneration, developer (see Glossary, Box 1), with the embryo developing into Central nervous system the worm form without passing through a swimming larval stage. In addition, P. dumerilii is a broadcast spawner whereas C. teleta Introduction retains the embryos in a brood tube, and leeches produce a cocoon. Notably, P. dumerilii is considered to be an errant annelid (see “You have made your way from worm to man, below), actively exploring the sea bed to scavenge and predate, and but much of you is still worm.” its morphology reflects this, with prominent jaws and an abundance Friedrich Nietzsche, Thus Spoke Zarathustra of sensory appendages and structures on its head and prominent (trans. R. J. Hollingdale, 1961) trunk appendages for gaining traction. By contrast, C. teleta The phylum Annelida gets its name from the latin ‘Anellus’ burrows around in the sediment much more and so has a more (meaning little ring) owing to the overt segmentation exhibited by ‘earthworm-like’ appearance, without prominent head or trunk most members of the group, a feature that annelids share with only appendages that would be a hindrance to this lifestyle. Leeches two other phyla, the arthropods (see Glossary, Box 1) and the provide a further contrast with the innovation of their anterior and chordates (see Glossary, Box 1) [also see Minelli (Minelli, 2004) posterior suckers, used for both locomotion and feeding. for a discussion of what is meant by ‘segmentation’]. The annelids This by no means covers all of the diversity within the annelids, are one of the few phyla that contains species occupying a range of and some of the other species used in evolutionary developmental habitats from marine to freshwater to terrestrial, although the biology studies, and which are mentioned elsewhere in this review, terrestrial species do only occupy rather damp terrestrial niches. are listed in Fig. 2 along with the phylogenetic relationships among This phylum includes the terrestrial earthworm, which was these taxa. Clearly there is a need for work in yet more species in championed by Charles Darwin to the extent that a cartoon order to represent properly the evolutionary diversity in the published in Punch’s Almanack (1882) declared “Man is but a annelids as well as to determine the ancestral states for various worm” (Box 2), as well as the blood-sucking leeches, the predatory developmental processes and features more reliably. ragworm often used as bait by fishermen, and the beautiful, majestic tube-building fanworms. Such a range of habitats along Recent developments in annelid phylogeny with a wide range of feeding strategies, including predation, deposit Understanding the relationships among a group of species within a feeding, filter feeding, parasitism and symbiosis, as well as the phylum, as well as the phylogenetic relationships relative to other unusual strategy adopted by the bone-eating snot-flower worm, phyla, is an essential prerequisite for any form of comparative, Osedax mucofloris (Glover et al., 2005), coincides with an evolutionary research, including evolutionary developmental impressive diversity of body forms and development. It is this biology. As segmentation is externally visible in both adult annelids diversity that makes the annelids a rich source of ‘material’ for and arthropods, traditional evolutionary scenarios and phylogenies investigating developmental mechanisms as well as the evolution of the animal kingdom proposed a sister group (see Glossary, Box of development. 1) relationship between these two phyla. They were known A variety of species are used in annelid evolutionary collectively as the Articulata, with the arthropods evolving from a developmental biology studies (some of which are shown in Fig. more annelid-like ancestor. With the advent of molecular 1), which is one of the strengths of this area of research and is phylogenetics, however, this sister group relationship was quickly essential for deducing accurate ancestral states for annelids as a abandoned (Field et al., 1988) and, whereas the Arthropoda have taken residence within the super-phylum Ecdysozoa (see Glossary, The Scottish Oceans Institute, the Gatty Marine Laboratory, University of St Box 1), alongside nematodes, onychophorans, priapulids and other Andrews, East Sands, St Andrews, Fife, KY16 8LB, UK. phyla, the Annelida have come to occupy a position within the *Author for correspondence ([email protected]) Lophotrochozoa (see Glossary, Box 1), alongside molluscs, DEVELOPMENT 2644 PRIMER Development 139 (15) Box 1. Glossary Box 2. Man is but a worm Arthropods. Members of the phylum Arthropoda, having a hard exoskeleton and jointed appendages. Includes insects such as Drosophila melanogaster, along with crustaceans, myriapods and chelicerates. Chordates. Members of the phylum Chordata, principally distinguished by the possession of a notochord at least at some point in their life cycle. Includes vertebrates, urochordates (e.g. Ciona intestinalis) and Cephalochordates (e.g. amphioxus). Clitellata. Annelids that possess a cocoon-forming clitellum, at least during the reproductive stages of their lives. Direct developers. Animals that do not possess a free larval stage that is distinct from the adult stage. Ecdysozoa. A super-phyletic clade of animals that periodically shed their cuticle (moult) via a process called ecdysis. Echinoderms. Members of the phylum Echinodermata, possessing a calcareous endoskeleton, water vascular system and pentaradial symmetry. Includes sea urchins, starfish, crinoids and sea cucumbers. Errantia. The clade of annelid families that tends to have an errant lifestyle, actively foraging over the sea-bed. Hemichordates. Members of the phylum Hemichordata. Marine benthic worms with pharyngeal gill slits and deuterostome development, but lacking a notochord. Includes the acorn worms (enteropneusts) and pterobranchs. Indirect developers. Animals that have a free larva that is distinct A cartoon from Punch’s Almanack for 1882 (published in Punch from the adult form and which usually undergoes some degree of Magazine on 6th December 1881) showing Darwin evolving from metamorphosis. chaos via an annelid worm, which in this case is his beloved Lophotrochozoa. A super-phyletic clade of animals that contains earthworm. At the time of this cartoon it was perhaps thought to phyla with either a lophophore (a ciliated, tentacular feeding be rather tongue-in-cheek, poking fun at the idea that something structure that also has a coelomic cavity derived from the middle as grand as a human could have arisen via evolution from such coelomic compartment, the mesocoel) and/or larvae based on the basic forms as worms. However, with modern discoveries in trochophore form (see main text). evolutionary developmental biology and genomics, the degree of Oligochaeta. Annelids with fewer, less pronounced chaetae than molecular similarity between animals such as humans and annelid polychaetes (see below) and no parapodia. worms is often surprising and undoubtedly more profound than Parapodia. The locomotory body appendages of polychaete many from the pre-molecular era would ever have imagined. annelids. Given the preponderance of worm-like forms across the animal Phylogenomics. The approach to building phylogenetic trees that kingdom, it is clear that the last common ancestor of annelids and uses genome-scale data sets, either from transcriptome or whole- humans will have been some sort of worm. Man is indeed but a genome data. rather fancy worm. Polychaeta. Annelids with many bristles, or chaetae, that are usually used for gaining traction during locomotion and often project from the ends of the parapodia. With the nesting of the annelids are often referred to as either errant (the Errantia, see clitellates within