Current genomic perspectives on animal diversity neglect two prominent phyla, the molluscs and annelids, that together account for nearly one-third of known marine species and are important both ...ecologically and as experimental systems in classical embryology. Here we describe the draft genomes of the owl limpet (Lottia gigantea), a marine polychaete (Capitella teleta) and a freshwater leech (Helobdella robusta), and compare them with other animal genomes to investigate the origin and diversification of bilaterians from a genomic perspective. We find that the genome organization, gene structure and functional content of these species are more similar to those of some invertebrate deuterostome genomes (for example, amphioxus and sea urchin) than those of other protostomes that have been sequenced to date (flies, nematodes and flatworms). The conservation of these genomic features enables us to expand the inventory of genes present in the last common bilaterian ancestor, establish the tripartite diversification of bilaterians using multiple genomic characteristics and identify ancient conserved long- and short-range genetic linkages across metazoans. Superimposed on this broadly conserved pan-bilaterian background we find examples of lineage-specific genome evolution, including varying rates of rearrangement, intron gain and loss, expansions and contractions of gene families, and the evolution of clade-specific genes that produce the unique content of each genome.
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DOBA, IJS, IZUM, KILJ, KISLJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Leeches are a unique group of annelids arising from an ancestor that would be characterized as a freshwater oligochaete worm. Comparative biology of the oligochaetes and the leeches reveals that body ...plan changes in the oligochaete‐to‐leech transition probably occurred by addition or modification of the terminal steps in embryonic development and that they were likely driven by a change in the feeding behavior in the ancestor of leeches. In this review article, developmental changes that are associated with the evolution of several leech‐specific traits are discussed. These include (1) the evolution of suckers, (2) the loss of chaetae, (3) the loss of septa, and (4) a fixed number of segments. An altered developmental fate of the teloblast is further proposed to be a key factor contributing to the fixation of the segment number, and the evolutionary change in teloblast development may also account for the loss of the ability to regenerate the lost body segments in the leech.
Comparative biology of the oligochaetes and the leeches reveals that body plan changes in the oligochaete‐to‐leech transition probably occurred by addition or modification of the terminal steps in embryonic development and that they were likely driven by a change in the feeding behavior in the ancestor of leeches. In this review article, developmental changes that are associated with the evolution of several leech‐specific traits are discussed.
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DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
In the animal kingdom, behavioral traits encompass a broad spectrum of biological phenotypes that have critical roles in adaptive evolution, but an EvoDevo approach has not been broadly used to study ...behavior evolution. Here, we propose that, by integrating two leech model systems, each of which has already attained some success in its respective field, it is possible to take on behavioral traits with an EvoDevo approach. We first identify the developmental changes that may theoretically lead to behavioral evolution and explain why an EvoDevo study of behavior is challenging. Next, we discuss the pros and cons of the two leech model species, Hirudo, a classic model for invertebrate neurobiology, and Helobdella, an emerging model for clitellate developmental biology, as models for behavioral EvoDevo research. Given the limitations of each leech system, neither is particularly strong for behavioral EvoDevo. However, the two leech systems are complementary in their technical accessibilities, and they do exhibit some behavioral similarities and differences. By studying them in parallel and together with additional leech species such as Haementeria, it is possible to explore the different levels of behavioral development and evolution.
Research Highlights
Behavior is a biological phenotype that can be studied by using an EvoDevo approach.
Changes in the neural circuits can result in behavioral change.
The leech Hirudo has been used to study neural circuits in the past half‐century.
Helobdella has been used to study leech development.
By comparing the different leeches, it is possible to characterize the molecular changes underlying changes in neural circuits and behavior.
As a direct developer, the entire course of development is experimentally tractable in the leech. This would provide a unique opportunity to study the EvoDevo of behaviors.
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DOBA, FZAB, GIS, IJS, IZUM, KILJ, NLZOH, NUK, OILJ, PILJ, PNG, SAZU, SBCE, SBMB, UILJ, UKNU, UL, UM, UPUK
•The polychaete-to-clitellate transition was a major event in annelid evolution.•Direct development emerged in the clitellate lineage.•Pattern of cell fate segregation is conserved between ...polychaetes and clitellates.•A heterochronic shift between cell lineages results in direct development.•Modularity in axial patterning mechanism enabled the heterochronic change.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Netrin is a remarkably conserved midline landmark, serving as a chemotactic factor that organizes the bilateral neural architecture in the post-gastrula bilaterian embryos. Netrin signal also guides ...cell migration in many other neural and non-neural organogenesis events in later developmental stages but has never been found to participate in gastrulation – the earliest cell migration in metazoan embryogenesis. Here, we found that the netrin signaling molecules and their receptors are expressed during gastrulation of the leech Helobdella. Intriguingly, Hau-netrin-1 was expressed in the N lineage, which gives rise in part to the ventral midline of ectoderm, at the onset of gastrulation. We demonstrated that the N lineage is required for the entrance of mesoderm into the germinal band and that misexpression of Hau-netrin-1 in early gastrulation prevented mesoderm from entering the germinal band. Together, these results suggested that Hau-netrin-1 secreted by the N lineage guides mesoderm migration during germinal band assembly. Furthermore, ectopic expression of Hau-netrin-1 after the completion of germinal band assembly disrupted the epibolic migration of the germinal bands in a later stage of gastrulation. Thus, Hau-netrin-1 is likely involved in two distinct events in sequential stages of leech gastrulation: the assembly of germinal bands in early gastrulation and their epibolic migration in mid-gastrulation. Given that the leech netrin is expressed in the precursor cells of the ventral midline during gastrulation, we propose that a heterochronic change from the midline netrin expression had taken place in the evolution of a novel mode of gastrulation in the directly developing leech embryos.
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•Netrin and netrin receptors are expressed during leech gastrulation.•Leech netrins are expressed in cell lineages contributing to future midline.•Netrin guides mesoderm migration during leech gastrulation.•Netrin may contribute to the evolution of a new mode of gastrulation.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Bone morphogenetic protein (BMP) signaling is broadly implicated in dorsoventral (DV) patterning of bilaterally symmetric animals 1–3, and its role in axial patterning apparently predates the birth ...of Bilateria 4–7. In fly and vertebrate embryos, BMPs and their antagonists (primarily Sog/chordin) diffuse and interact to generate signaling gradients that pattern fields of cells 8–10. Work in other species reveals diversity in essential facets of this ancient patterning process, however. Here, we report that BMP signaling patterns the DV axis of segmental ectoderm in the leech Helobdella, a clitellate annelid (superphylum Lophotrochozoa) featuring stereotyped developmental cell lineages, but the detailed mechanisms of DV patterning in Helobdella differ markedly from fly and vertebrates. In Helobdella, BMP2/4s are expressed broadly, rather than in dorsal territory, whereas a dorsally expressed BMP5–8 specifies dorsal fate by short-range signaling. A BMP antagonist, gremlin, is upregulated by BMP5–8 in dorsolateral, rather than ventral territory, and yet the BMP-antagonizing activity of gremlin is required for normal ventral cell fates. Gremlin promotes ventral fates without disrupting dorsal fates by selectively inhibiting BMP2/4s, not BMP5–8. Thus, DV patterning in the development of the leech revealed unexpected evolutionary plasticity of the conserved BMP patterning system, presumably reflecting its adaptation to different modes of embryogenesis.
► BMP patterns “O-P equivalence group” of leech segmental ectoderm ► Dorsally expressed BMP5–8 upregulates gremlin expression in P lineage ► Gremlin tunes down activity of broadly expressed BMP2/4 and is required for O fate ► BMP5–8, not sensitive to gremlin, produces high signaling activity in P lineage
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Glossiphoniid leeches of the genus Helobdella provide experimentally tractable models for studies in evolutionary developmental biology (Evo-Devo). Here, after a brief rationale, we will summarize ...our current understanding of Helobdella development and highlight the near term prospects for future investigations, with respect to the issues of: D quadrant specification; the transition from spiral to bilaterally symmetric cleavage; segmentation, and the connections between segmental and non-segmental tissues; modifications of BMP signaling in dorsoventral patterning and the O-P equivalence group; germ line specification and genome rearrangements. The goal of this contribution is to serve as a summary of, and guide to, published work.
In the leech Helobdella, the ectoderm exhibits a high degree of morphological homonomy between body segments, but pattern elements in lateral ectoderm arise via distinct cell lineages in the segments ...of the rostral and midbody regions. In each of the four rostral segments, a complete set of ventrolateral (O fate) and dorsolateral (P fate) ectodermal pattern elements arises from a single founder cell, op. In the 28 midbody and caudal segments, however, there are two initially indeterminate o/p founder cells; the more dorsal of these is induced to adopt the P fate by BMP5–8 emanating from the dorsalmost ectoderm, while the more ventral cell assumes the O fate. Previous work has suggested that the dorsoventral patterning of O and P fates differs in the rostral region, but the role of BMP signaling in those segments has not been investigated. We show here that suppression of dorsal BMP5–8 signaling (which effects a P-to-O fate change in the midbody) has no effect on the patterning of O and P fates in the rostral region. Furthermore, ectopic expression of BMP5–8 in the ventral ectoderm (which induces an O-to-P fate change in the midbody) has no effect in the rostral region. Finally, expression of a dominant-negative BMP receptor (which induces a P-to-O fate change in the midbody) fails to affect O/P patterning in the rostral region. Thus, the rostral segments appear to use some mechanism other than BMP signaling to pattern O and P cell fates along the dorsoventral axis. From a mechanistic standpoint, the OP lineage of the rostral segments and the O–P equivalence group of the midbody and caudal segments constitute distinct developmental modules that rely to differing degrees on positional cues from surrounding ectoderm in order to specify homonomous cell fates.
► Segmented leech body plan comprises rostral, midbody and caudal regions. ► BMP signaling is required for DV patterning in midbody lateral ectoderm. ► BMP signaling is dispensable for patterning rostral lateral ectoderm. ► This regional difference reflects modular nature of segmental units in leech.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
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