Publications

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2017
Holland, ND, Holland LZ.  2017.  The ups and downs of amphioxus biology: a history. International Journal of Developmental Biology. 61:575-583.   10.1387/ijdb.160395LH   AbstractWebsite

Humans (at least a select few) have long known about the cephalochordate amphioxus, first as something to eat and later as a subject for scientific study. The rate of publication on these animals has waxed and waned several times. The first big surge, in the late nineteenth century, was stimulated by Darwin's evolutionary ideas and by Kowalevsky's embryologic findings suggesting that an amphioxus-like creature might have bridged the gap between the invertebrates and the vertebrates. Interest declined sharply in the early twentieth century and remained low for the next 50 years. An important contributing factor (in addition to inhibition by two world wars and the Great Depression) was the indifference of the new evolutionary synthesis toward broad phylogenetic problems like the origin of the vertebrates. Then, during the 1960s and 1970s, interest in amphioxus resurged, driven especially by increased government support for basic science as well as opportunities presented by electron microscopy. After faltering briefly in the 1980s (electron microscopists were running out of amphioxus tissues to study), a third and still-continuing period of intensive amphioxus research began in the early 1990s, stimulated by the advent of evolutionary developmental biology (evo-devo) and genomics. The volume of studies peaked in 2008 with the publication of the genome of the Florida amphioxus. Since then, although the number of papers per year has dropped somewhat, sequencing of additional genomes and transcriptomes of several species of amphioxus (both in the genus Branchiostoma and in a second genus, Asymmetron) is providing the raw material for addressing the major unanswered question of the relationship between genotype and phenotype.

2013
Holland, LZ, Carvalho JE, Escriva H, Laudet V, Schubert M, Shimeld SM, Yu JK.  2013.  Evolution of bilaterian central nervous systems: a single origin? Evodevo. 4   10.1186/2041-9139-4-27   AbstractWebsite

The question of whether the ancestral bilaterian had a central nervous system (CNS) or a diffuse ectodermal nervous system has been hotly debated. Considerable evidence supports the theory that a CNS evolved just once. However, an alternative view proposes that the chordate CNS evolved from the ectodermal nerve net of a hemichordate-like ancestral deuterostome, implying independent evolution of the CNS in chordates and protostomes. To specify morphological divisions along the anterior/posterior axis, this ancestor used gene networks homologous to those patterning three organizing centers in the vertebrate brain: the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer, and subsequent evolution of the vertebrate brain involved elaboration of these ancestral signaling centers; however, all or part of these signaling centers were lost from the CNS of invertebrate chordates. The present review analyzes the evidence for and against these theories. The bulk of the evidence indicates that a CNS evolved just once - in the ancestral bilaterian. Importantly, in both protostomes and deuterostomes, the CNS represents a portion of a generally neurogenic ectoderm that is internalized and receives and integrates inputs from sensory cells in the remainder of the ectoderm. The expression patterns of genes involved in medio/lateral (dorso/ventral) patterning of the CNS are similar in protostomes and chordates; however, these genes are not similarly expressed in the ectoderm outside the CNS. Thus, their expression is a better criterion for CNS homologs than the expression of anterior/posterior patterning genes, many of which (for example, Hox genes) are similarly expressed both in the CNS and in the remainder of the ectoderm in many bilaterians. The evidence leaves hemichordates in an ambiguous position - either CNS centralization was lost to some extent at the base of the hemichordates, or even earlier, at the base of the hemichordates + echinoderms, or one of the two hemichordate nerve cords is homologous to the CNS of protostomes and chordates. In any event, the presence of part of the genetic machinery for the anterior neural ridge, the zona limitans intrathalamica and the isthmic organizer in invertebrate chordates together with similar morphology indicates that these organizers were present, at least in part, at the base of the chordates and were probably elaborated upon in the vertebrate lineage.

2008
Holland, LZ, Holland ND, Gilland E.  2008.  Amphioxus and the evolution of head segmentation. Integrative and Comparative Biology. 48:630-646.   10.1093/icb/icn060   AbstractWebsite

Whether or not the vertebrate head is fundamentally segmented has been controversial for over 150 years. Beginning in the late 19th century, segmentalist theories proposed that the vertebrate head evolved from an amphioxus-like ancestor in which mesodermal somites extended the full length of the body with remnants of segmentation persisting as the mesodermal head cavities of sharks and lampreys. Antisegmentalists generally argued either that the vertebrate ancestors never had any mesodermal segmentation anteriorly or that they lost it before the origin of the vertebrates; in either case, the earliest vertebrates had an unsegmented head and the embryonic cranial mesoderm of vertebrates is at best pseudo-segmented, evolving independently of any pre-vertebrate segmental pattern. Recent morphologic studies have generally confirmed the accuracy of the major classical studies of head development in lampreys and sharks, yet disagree with their theoretical conclusions regarding the evolution of head segmentation. Studies of developmental genes in amphioxus and vertebrates, which have demonstrated conservation of the mechanisms of anteriorposterior patterning in the two groups, have shed new light on this controversy. Most pertinently, some homologs of genes expressed in the anterior amphioxus somites, which form as outpocketings of the gut, are also expressed in the walls of the head cavities of lampreys, which form similarly, and in their major derivatives (the velar muscles) as well as in the eye and jaw muscles of bony gnathostomes, which derive from unsegmented head mesoderm. These muscles share gene expression with the corresponding muscles of the shark, which derive from the walls of head cavities that form, not as outpocketings of the gut, but as secondary cavities within solid blocks of tissue. While molecular data that can be compared across all the relevant taxa remain limited, they are consistent with an evolutionary scenario in which the cranial paraxial mesoderm of the lamprey and shark evolved from the anterior somites of an amphioxus-like ancestor. Although, bony vertebrates have lost the mesodermal head segments present in the shark and lamprey, their remnants persist in the muscles of the eye and jaw.

2007
Beaster-Jones, L, Schubert M, Holland LZ.  2007.  Cis-regulation of the amphioxus engrailed gene: Insights into evolution of a muscle-specific enhancer. Mechanisms of Development. 124:532-542.   10.1016/j.mod.2007.06.002   AbstractWebsite

To gain insights into the relation between evolution of cis-regulatory DNA and evolution of gene function, we identified tissue-specific enhancers of the engrailed gene of the basal chordate amphioxus (Branch iostoma floridae) and compared their ability to direct expression in both amphioxus and its nearest chordate relative, the tunicate Ciona intestinalis. In amphioxus embryos, the native engrailed gene is expressed in three domains - the eight most anterior somites, a few cells in the central nervous system (CNS) and a few ectodermal cells. In contrast, in C. intestinalis, in which muscle development is highly divergent, engrailed expression is limited to the CNS. To characterize the tissue-specific enhancers of amphioxus engrailed, we first showed that 7.8 kb of upstream DNA of amphioxus engrailed directs expression to all three domains in amphioxus that express the native gene. We then identified the amphioxus engrailed muscle-specific enhancer as the 1.2 kb region of upstream DNA with the highest sequence identity to the mouse en-2 jaw muscle enhancer. This amphioxus enhancer directed expression to both the somites in amphioxus and to the larval muscles in C intestinalis. These results show that even though expression of the native engrailed has apparently been lost in developing C intestinalis muscles, they express the transcription factors necessary to activate transcription from the amphioxus engrailed enhancer, suggesting that gene networks may not be completely disrupted if an individual component is lost. (c) 2007 Elsevier Ireland Ltd. All rights reserved.

2006
Schubert, M, Holland ND, Laudet V, Holland LZ.  2006.  A retinoic acid-Hox hierarchy controls both anterior/posterior patterning and neuronal specification in the developing central nervous system of the cephalochordate amphioxus. Developmental Biology. 296:190-202.   10.1016/j.ydbio.2006.04.457   AbstractWebsite

Retinoic acid (RA) mediates both anterior/posterior patterning and neuronal specification in the vertebrate central nervous system (CNS). However, the molecular mechanisms downstream of RA are not well understood. To investigate these mechanisms, we used the invertebrate chordate amphioxus, in which the CNS, although containing only about 20,000 neurons in adults, like the vertebrate CNS, has a forebrain, midbrain, hindbrain, and spinal cord and is regionalized by RA-signaling. Here we show, first, that domains of genes with expression normally limited to diencephalon and midbrain are generally not affected by altered RA-signaling, second, that contrary to previous reports, not only Hox1, 3, and 4, but also Hox2 and Hox6 are collinearly expressed in the amphioxus CNS, and third, that collinear expression of all these Hox genes is controlled by RA-signaling. Finally, we show that Hox1 is involved in mediating both the role of RA-signaling in regionalization of the hindbrain and in specification of hindbrain motor neurons. Thus, morpholino knock-down of the single amphioxus Hox1 mimics the effects of treatments with an RA-antagonist. This analysis establishes RA-dependent regulation of collinear Hox expression as a feature common to the chordate CNS and indicates that the RA-Hox hierarchy functions both in proper anterior/posterior patterning of the developing CNS and in specification of neuronal identity. (c) 2006 Elsevier Inc. All rights reserved.