Publications

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2015
Holland, LZ.  2015.  Evolution of basal deuterostome nervous systems. Journal of Experimental Biology. 218:637-645.   10.1242/jeb.109108   AbstractWebsite

Understanding the evolution of deuterostome nervous systems has been complicated by the by the ambiguous phylogenetic position of the Xenocoelomorpha (Xenoturbellids, acoel flat worms, nemertodermatids), which has been placed either as basal bilaterians, basal deuterostomes or as a sister group to the hemichordate/echinoderm clade (Ambulacraria), which is a sister group of the Chordata. None of these groups has a single longitudinal nerve cord and a brain. A further complication is that echinoderm nerve cords are not likely to be evolutionarily related to the chordate central nervous system. For hemichordates, opinion is divided as to whether either one or none of the two nerve cords is homologous to the chordate nerve cord. In chordates, opposition by two secreted signaling proteins, bone morphogenetic protein (BMP) and Nodal, regulates partitioning of the ectoderm into central and peripheral nervous systems. Similarly, in echinoderm larvae, opposition between BMP and Nodal positions the ciliary band and regulates its extent. The apparent loss of this opposition in hemichordates is, therefore, compatible with the scenario, suggested by Dawydoff over 65 years ago, that a true centralized nervous system was lost in hemichordates.

2010
Holland, ND, Holland LZ.  2010.  Laboratory Spawning and Development of the Bahama Lancelet, Asymmetron lucayanum (Cephalochordata): Fertilization Through Feeding Larvae. Biological Bulletin. 219:132-141. AbstractWebsite

Here we report on spawning and development of the Bahama lancelet, Asymmetron lucayanum. Ripe adults collected in Bimini spawned the same evening when placed in the dark for 90 minutes. The developmental morphology is described from whole mounts and histological sections. A comparison between development in A symmetron and the better known cephalochordate genus Branchiostoma reveals similarities during the early embryonic stages but deviations by the late embryonic and early larval stages. Thus, the initial positions of the mouth, first gill slit, and anus differ between the two genera. Even more strikingly, Hatschek's right and left diverticula, which arise by enterocoely at the anterior end of the pharynx in Branchiostoma, never form during Asymmetron development. In Branchiostoma, these diverticula become the rostral coelom and preoral pit. In Asymmetron, by contrast, homologs of the rostral coelom and preoral pit form by schizocoely within an anterior cell cluster of unproven (but likely endodermal) origin. Proposing evolutionary scenarios to account for developmental differences between Asymmetron and Branchiostoma is currently hampered by uncertainty over which genus is basal in the cephalochordates. A better understanding of developmental diversity within the cephalochordates will require phylogenetic analyses based on nuclear genes and the genome sequence of an Asymmetron species.

2007
Holland, LZ, Holland ND.  2007.  A revised fate map for amphioxus and the evolution of axial patterning in chordates. Integrative and Comparative Biology. 47:360-372.   10.1093/icb/icm064   AbstractWebsite

The chordates include vertebrates plus two groups of invertebrates (the cephalochordates and tunicates). Previous embryonic fate maps of the cephalochordate amphioxus (Branchiostoma) were influenced by preconceptions that early development in amphioxus and ascidian tunicates should be fundamentally the same and that the early amphioxus embryo, like that of amphibians, should have ventral mesoderm. Although detailed cell lineage tracing in amphioxus has not been done because of limited availability of the embryos and because cleavage is radial and holoblastic with the blastomeres nearly equal in size and not tightly adherent until the mid-blastula stage, a compilation of data from gene expression and function, blastomere isolation and dye labeling allows a more realistic fate map to be drawn. The revised fate map is substantially different from that of ascidians. It shows (1) that the anterior pole of the amphioxus embryo is offset dorsally from the animal pole only by about 20 degrees, (2) that the ectoderm/mesendoderm boundary (the future rim of the blastopore) is at the equator of the blastula, which approximately coincides with the 3rd cleavage plane, and (3) that there is no ventral mesoderm during the gastrula stage. Involution or ingression of cells over the blastopore lip is negligible, and the blastopore, which is posterior, closes centripetally as if by a purse string. During the gastrula stage, the animal pole shifts ventrally, coming to lie about 20 degrees ventral to the anterior tip of the late gastrula/early neurula. Comparisons of the embryos of amphioxus and vertebrates indicate that in spite of large differences in the mechanics of cleavage and gastrulation, anterior/posterior and dorsal/ventral patterning occur by homologous genetic mechanisms. Therefore, the small, nonyolky embryo of amphioxus is probably a reasonable approximation of the basal chordate embryo before the evolution of determinate cleavage in the tunicates and the evolution large amounts of yolk in basal vertebrates.

Yu, JK, Satou Y, Holland ND, Shin-I T, Kohara Y, Satoh N, Bronner-Fraser M, Holland LZ.  2007.  Axial patterning in cephalochordates and the evolution of the organizer. Nature. 445:613-617.   10.1038/nature05472   AbstractWebsite

The organizer of the vertebrate gastrula is an important signalling centre that induces and patterns dorsal axial structures. Although a topic of long-standing interest, the evolutionary origin of the organizer remains unclear. Here we show that the gastrula of the cephalochordate amphioxus expresses dorsal/ventral (D/V) patterning genes (for example, bone morphogenetic proteins (BMPs), Nodal and their antagonists) in patterns reminiscent of those of their vertebrate orthlogues, and that amphioxus embryos, like those of vertebrates, are ventralized by exogenous BMP protein. In addition, Wnt-antagonists (for example, Dkks and sFRP2-like) are expressed anteriorly, whereas Wnt genes themselves are expressed posteriorly, consistent with a role for Wnt signalling in anterior/posterior (A/P) patterning. These results suggest evolutionary conservation of the mechanisms for both D/V and A/P patterning of the early gastrula. In light of recent phylogenetic analyses placing cephalochordates basally in the chordate lineage, we propose that separate signalling centres for patterning the D/V and A/P axes may be an ancestral chordate character.

2003
Mazet, F, Yu JK, Liberles DA, Holland LZ, Shimeld SM.  2003.  Phylogenetic relationships of the Fox (Forkhead) gene family in the Bilateria. Gene. 316:79-89.   10.1016/s0378-1119(03)00741-8   AbstractWebsite

The Forkhead or Fox gene family encodes putative transcription factors. There are at least four Fox genes in yeast, 16 in Drosophila melanogaster (Dm) and 42 in humans. Recently, vertebrate Fox genes have been classified into 17 groups named FoxA to FoxQ [Genes Dev. 14 (2000) 142]. Here, we extend this analysis to invertebrates, using available sequences from D. melanogaster, Anopheles gambiae (Ag), Caenorhabditis elegans (Ce), the sea squirt Ciona intestinalis (Ci) and amphioxus Branchiostoma floridae (Bf), from which we also cloned several Fox genes. Phylogenetic analyses lend support to the previous overall subclassification of vertebrate genes, but suggest that four subclasses (FoxJ, L, N and Q) could be further subdivided to reflect their relationships to invertebrate genes. We were unable to identify orthologs of Fox subclasses E, H, I, J, M and Q1 in D. melanogaster, A. gambiae or C. elegans, suggesting either considerable loss in ecdysozoans or the evolution of these subclasses in the deuterostome lineage. Our analyses suggest that the common ancestor of protostomes and deuterostomes had a minimum complement of 14 Fox genes. (C) 2003 Elsevier B.V. All rights reserved.