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[
Bioessays,
2008]
Homology is the similarity between organisms due to common ancestry. Introduced by Richard Owen in 1843 in a paper entitled "Lectures on comparative anatomy and physiology of the invertebrate animals", the concept of homology predates Darwin's "Origin of Species" and has been very influential throughout the history of evolutionary biology. Although homology is the central concept of all comparative biology and provides a logical basis for it, the definition of the term and the criteria of its application remain controversial. Here, I will discuss homology in the context of the hierarchy of biological organization. I will provide insights gained from an exemplary case study in evolutionary developmental biology that indicates the uncoupling of homology at different levels of biological organization. I argue that continuity and hierarchy are separate but equally important issues of homology.
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[
Dev Suppl,
1994]
The invariant development of free-living nematodes combined with the extensive knowledge of Caenorhabditis elegans developmental biology provides an experimental system for an analysis of the evolution of developmental mechanisms. We have collected a number of new nematode species from soil samples. Most are easily cultured and their development can be analyzed at the level of individual cells using techniques standard to Caenorhabditis. So far, we have focused on differences in the development of the vulva among species of the families Rhabditidae and Panagrolaimidae. Preceding vulval development, twelve Pn cells migrate into the ventral cord and divide to produce posterior daughters [Pn.p cells] whose fates vary in a position specific manner [from P1.p anterior to P12.p posterior]. In C. elegans hermaphrodites, P(3-8).p are tripotent and from an equivalence group. These cells can express either of two vulval fates (1 or 2) in response to a signal from the anchor cell of the somatic gonad, or a non-vulval fate (3), resulting in a 3-3-2-1-2-3 pattern of cell fates. Evolutionary differences in vulval development include the number of cells in the vulval equivalence group, the number of 1 cells, the number of progeny generated by each vulval precursor cell, and the position of VPCs before morphogenesis. Examples of three Rhabditidae genera have a posterior vulva in the position of P9-P11 ectoblasts. In Cruznema tripartitum, P(5-7).p form the vulva as in Caenorhabditis, but they migrate posteriorly before dividing. Induction occurs after the gonad grows posteriorly to the position of P(5-7).p cells. In two other species, Mesorhabditis sp. PS 1179 and Teratorhabditis palmarum, we have found changes in induction and competence with respect to their presumably more C. elegans-like ancestor. In Mesorhabditis, P(5-7).p form the vulva after migrating to a posterior position. However, the gonad is not required to specify the pattern of cell fates 3-2-1-2-3. Moreover, the Pn.p cells are not equivalent in their potentials to form the vulva. A regulatory constraint in this family thus forces the same set of precursors to generate the vulva, rather than more appropriately positioned Pn.p cells.
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[
Curr Biol,
2000]
Recent studies have introduced Oscheius sp. CEW1 as a third nematode species accessible to genetic analysis, joining the better known Caenorhabditis elegans and Pristionchus pacificus. A group of vulva-defective mutants in Oscheius has been identified, with defects not seen in C. elegans.
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[
Invertebrate Reproduction and Development,
1999]
Over the last few years vulva development in nematodes has been used as a model system to study the evolution of developmental processes by carrying out cell lineage and cell ablation studies in various nematodes. Furthermore, a genetic and molecular analysis of vulva development has been initiated in Pristionchus pacificus. Evolutionary interpretation of these comparative developmental studies requires a phylogenetic understanding of nematodes. Recently, a molecular phylogeny for the phylum Nematoda has been published. Here, we place the comparative data of vulva development onto this phylogeny of nematodes to infer the direction of evolutionary change.
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[
Mol Ecol,
2013]
Comprehensive studies of evolution have historically been hampered by the division among disciplines. Now, as biology moves towards an '-omics' era, it is more important than ever to tackle the evolution of function and form by considering all those research areas involved in the regulation of phenotypes. Here, we review recent attempts to establish the nematode Pristionchus pacificus as a model organism that allows integrative studies of development and evo-devo, with ecology and population genetics. Originally developed for comparative study with the nematode Caenorhabditis elegans, P.pacificus provided insight into developmental pathways including dauer formation, vulva and gonad development, chemosensation, innate immunity and neurobiology. Its subsequent discovery across a wide geographic distribution in association with scarab beetles enabled its evaluation in a biogeographic context. Development of an evolutionary field station on La Reunion Island, where P.pacificus is present in high abundance across a number of widespread habitat types, allows examination of the microfacets of evolution - processes of natural selection, adaptation and drift among populations can now be examined in this island setting. The combination of laboratory-based functional studies with fieldwork in P.pacificus has the long-term prospective to provide both proximate (mechanistic) and ultimate (evolutionary and ecological) causation and might therefore help to overcome the long-term divide between major areas in biology.
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[
Science,
1994]
In Caenorhabditis, the vulva is formed in the central body region from three of six equivalent cells and is induced by the gonad. In some nematodes, however, the vulva is located in the posterior body region. Vulval development has been analyzed in three such genera. The same precursor cells give rise to the vulva in Caenorhabditis and in the posterior vulva species, but in the latter the cells first migrate posteriorly. In two such species, the vulva is not induced by the gonad, but instead relies on intrinsic properties of precursor cells. Thus, evolution of organ position involves changes in induction and competence.
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[
Adv Exp Med Biol,
2012]
Changes in the developmental processes and developmental mechanisms can result in the modification of morphological structures and in the evolution of phenotypic novelty. But how do developmental processes evolve? One striking finding in modern biology is the confrontation of morphological diversity in multicellular organisms with the conserved blueprint of life-the small number of conserved signaling pathways and transcriptional regulators. Evolutionary developmental biology (evo-devo) tries to explain this discrepancy between macroscopic diversity and molecular uniformity. Selected case studies in evo-devo models allowed detailed insight into the mechanisms of evolutionary changes and might help solving this problem. Here, I compare the formation of vulva development between Caenorhabditis elegans and the evo-devo model Pristionchus pacificus. More than 3 decades of work in C. elegans and 15 years in P. pacificus provide an insight into the molecular mechanisms of developmental change during vulva evolution. C. elegans and P. pacificus differ first, in the type of the signaling system used for vulva induction; second, the cells required for the inductive interactions; third, the logic of the signal system, and finally, the sequence and structure of peptide domains in otherwise conserved proteins. Nonetheless, the vulva is formed from the same three cells in both nematodes. I discuss redundancy as an evolutionary mechanism to explain developmental systems drift, a theory predicting conserved morphological structures to be generated by diverse molecular regulatory networks.
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[
Development,
1997]
The origin of novelty is one of the least understood evolutionary phenomena. One approach to study evolutionary novelty comes from developmental biology. During developmental cell fate specification of the nematode Pristionchus pacificus (Diplogastridae), five cell fates can be distinguished within a group of twelve ventral epidermal cells. The differentiation pattern of individual cells includes programmed cell death, cell fusion and vulval differentiation after induction by the gonad. A cell lineage comparison among species of seven different genera of the Diplogastridae indicates that the differentiation pattern of ventral epidermal cells is highly conserved. Despite this morphological conservation, cell ablation experiments indicate many independent alterations of underlying mechanisms of cell fate specification. Cell fusion and individual cell competence change during evolution as well as the differentiation property in response to inductive signaling. These results suggest that developmental mechanisms, some of which are redundantly involved in vulval fate specification of the genetic model organism Caenorhabditis elegans, can evolve without concomitant morphological change.
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[
Fundamental and Applied Nematology,
1996]
We describe a new free-living hermaphroditic nematode, Pristionchus pacificus sp. n. (Neodiplogastridae) that will be useful for genetic, developmental and molecular biological studies. P. pacificus sp. n. has six chromosomes, a three day generation time and is easily cultured. Forty-eight morphological mutations are described indicating the genetic accessibility. Molecular studies have been initiated with the generation of a genomic and a cDNA library and the cloning of the homologue of the Caenorhabditis elegans
let-60 ras gene.
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[
Dev Biol,
1995]
During the formation of the vulva in many nematode hermaphrodites or females, pattern formation, induction, and cell specification can readily be studied at a single-cell level. Nematodes thus allow an evolutionary analysis of developmental processes. We have analyzed cell lineages and pattern formation in the vulva equivalence group of six rhabditid nematodes of the genera Oscheius, Rhabditella, Rhabditoides, Pelodera, and Protorhabditis. The comparison of these species with four previously analyzed species of this family reveals evolutionary modification at several levels. The number of vulva precursor cells (VPCs) differ among species. Of the three particular cell lineages (1 degrees, 2 degrees, and 3 degrees) generated by the vulva precursor cells in Caenorhabditis, two (2 degrees and 3 degrees) are altered, whereas the third lineage (1 degrees) is conserved among the analyzed species. While most vulval lineages are invariant, we observe variability of the 3 degrees lineage in Pelodera with respect to the number of precursor cells adopting this fate and the number of progeny formed. In two species, the 3 degrees lineage generates an asymmetrical set of cells, oriented by the gonad. In Protorhabditis we frequently find animals with an additional or altered set