Homology and homoeomorphy in ostracod limbs

The functional modifications of myodocopan and podocopan ostracod limbs constitute a rich data set with which to carry out phylogenetic analyses, but efforts are hindered by lack of consensus on homologies. Homoeomorphy presents particular difficulties; for example, the furca is post-anal in Myodocopa but pre-anal in Podocopa, suggesting homoeomorphy, not homology. Homoeomorphies also exist between ostracod appendages and those of other Crustacea, for example the oral cone and styliform mandibulae of Paradoxostomatidae (Ostracoda) and Siphonostomatoida (Copepoda), both adaptations to commensal or parasitic lifestyles. Such clear manifestations of homoeomorphy, arising independently in different lineages as a result of similar functional requirements imposed on plesiomorphic appendage structures, warn of the possibility of more subtle examples which, if unrecognized, would lead to misinterpretations of character states used in phylogenetic analysis. For instance, the branchial plates found on third, fourth and fifth limbs of podocopans may not be homologous with the branchial plates on the fifth and sixth limbs of myodocopans. Limb homologies of podocopan ostracods (primarily as represented by various podocopid taxa) are investigated. Evidence is presented, based on studies of morphology and musculature, that podocopid branchial plates are exopodites (arising from the basis), while those of myodocopans are epipodites (arising from the coxa or precoxa). In Podocopida, moreover, the protopodites of post-mandibular limbs appear to be undifferentiated, comprising only a basis, while those of Myodocopa clearly exhibit a basis, coxa and often a precoxa. These differences argue against monophyly of the Ostracoda. The absence of epipodites, combined with the lack of a coxa in post-mandibular limbs, is potentially indicative of closer affinities between podocopans and Cambrian stem-group crustaceans (including Phosphatocopida) than between podocopans and myodocopans. The possible derivation of podocopid third, fourth and fifth limbs from a stem-group crustacean limb is demonstrated. The hypothesis is advanced that podocopan ostracods (represented today by Podocopida, Platycopida and Palaeocopida) are derived from much nearer the base of the crown-group Crustacea than myodocopans.     

Reconstructing serial homology with a special emphasis on the nature of limbs in vertebrates and with references to Cruveilhier,Wyman, Belogolowy,and Balinsky

This analysis was inspired by the recent paper by Siomava et al. (2020) who attempted to deconstruct the serial homology concept, but retain the special homology. The criticism against this attempt is presented based on reconsideration of the original Owen's trinitarian concept of the general, serial, and special homology, and on a number of evidence on the vertebrate limbs serial homologies and on the vertebrate occiput special homologies which are currently missed by the morphologist community. The research of Belogolowy (1911) proved that the concept of special homology can be deconstructed with the same reasoning as suggested by Siomava et al. (2020) against the serial homology concept. It is argued that the deconstruction attempts come from wrong expectations in respect of homology. It is argued, that, due to developmental singularities, such as the zygote, or spore, or bud (in vegetative reproduction), the true homogeny is possible for genes only. The organs do not arise from organs, and therefore their genetic basis, and hence homology, can be changed in the developmental singularities. Thus, the morphological homology is not static. It can be acquired and it can evolve. Genetically, the evolution of morphological homologies can be thought of as a succession of co-options. The evidence for a succession of serial homologies in vertebrate limbs is suggested. It is argued that homology and analogy have a sense only in relation to each other. When two correspondences between two organs exist simultaneously, the older (deeper in time) is homology, and the newer (more superficial) is analogy. In this conceptual framework of evolvable homology, neither of the three Owen's types of homology can be abandoned. Three respective types of analogy should be added—the general analogy, the serial analogy, and the special analogy.     

Morphogenic machines evolve more rapidly than the signals that pattern them: lessons from amphibians

The induction of mesoderm and the patterning of its dorsal-ventral and anterior-posterior axes seems to be relatively conserved throughout the chordates, as do the morphogenic movements that produce a phylotypic stage embryo. What is not conserved is the initial embryonic architecture of the fertilized egg, and the specific cell behaviors used to drive mesoderm morphogenesis. How then do conserved patterning pathways adapt to diverse architectures and where do they diverge to direct the different cell behaviors used to shape the phylotypic body plan? Amphibians in particular, probably because of their broad range of reproductive strategies, show diverse embryonic architectures across their class and use diverse cell behaviors during their early morphogenesis, making them an interesting comparative group. We examine three examples from our work on amphibians that show variations in the use of cell behaviors to drive the morphogenesis of the same tissues. We also consider possible points where the conserved patterning pathways might diverge to produce different cell behaviors.     

Mesenchymal cell polarity and morphogenesis of chick cartilage

Mesenchymal cell polarity was studied in the developing cartilages of chick vertebral bodies and limbs using a silver impregnation technique for the Golgi apparatus. Distinct patterns of cell orientation are apparent in the cells at a number of different stages of morphogenesis. The data support the hypothesis that individual cells are inherently polarized, and that morphogenesis of multicellular patterns results from the coordinated three-dimensional orientation of anisotropic cells.     

From head to toe: conservation of molecular signals regulating limb and craniofacial morphogenesis

Recent evidence indicates that many molecules involved in generating and patterning the limbs also play a role during craniofacial morphogenesis. On the surface, this is an unexpected finding given that these regions of the body have separate evolutionary origins, are composed of different embryonic tissues, and are quite dissimilar in their anatomy. Results from several experiments involving Sonic hedgehog and retinoic acid point to a remarkable conservation of the signaling pathways mediated by these morphogens across multiple organ systems. Moreover, mutants such as the extra-toes and doublefoot mouse, and the talpid chicken also provide insights on common developmental processes that underlie the formation of the limbs and face. The identification of highly conserved aspects of morphogenesis is important for understanding fundamental mechanisms of development, as well as for revealing the common denominator of countless birth defects and providing new strategies for their prevention and cure.     

A good eye for arthropod evolution

Insect and crustacean lineages diverged over 500 Myr ago, and there are continuing uncertaintles about whether they evolved from a common arthropod ancestor or, alternatively, they evolved independently from annelid worms. Despite the diversity of their limbs and lifestyles, the nervous systems of insects and crustaeeans share many common features both in development and in function. Cellular and molecular embryology techniques reveal good evidence for homologies in the developing segmental ganglia. In the visual system, this seemingly common programme of insect and crustacean CNS development culminates in common adult neural function. Comparisons of the cellular anatomy and physiology of animals as diverse as flies and crayfishes indicate that the neural circuits in the lamina of their optic lobe have been inherited largely unchanged from a common ancestor with good compound eyes.     

Structure and development of setae on the thoracic limbs of the anostracan crustacean, Thamnocephalus platyurus

Setae are a prominent feature of arthropod limbs. In taxa where the limbs develop during the larval phase, developing setae are an integral part of the developing limb bud and their differentiation cannot easily be separated from the early patterning and formation of the overall limb. Here I describe the morphogenesis and adult setae in a branchiopod crustacean, the anostracan, Thamnocephalus platyurus. The majority of the setae on the limbs are non-innervated plumose setae that are formed from six underlying cells. Because branchiopods are often sampled in comparative studies of limb development, the details of the cellular morphogenesis of their limbs provide a necessary basis for studies of limb patterning.     

Internalization of multiple cells during C. elegans gastrulation depends on common cytoskeletal mechanisms but different cell polarity and cell fate regulators

Understanding the links between developmental patterning mechanisms and force-producing cytoskeletal mechanisms is a central goal in studies of morphogenesis. Gastrulation is the first morphogenetic event in the development of many organisms. Gastrulation involves the internalization of surface cells, often driven by the contraction of actomyosin networks that are deployed with spatial precision—both in specific cells and in a polarized manner within each cell. These cytoskeletal mechanisms rely on different cell fate and cell polarity regulators in different organisms. Caenorhabditis elegans gastrulation presents an opportunity to examine the extent to which diverse mechanisms may be used by dozens of cells that are internalized at distinct times within a single organism. We identified 66 cells that are internalized in C. elegans gastrulation, many of which were not known previously to gastrulate. To gain mechanistic insights into how these cells internalize, we genetically manipulated cell fate, cell polarity and cytoskeletal regulators and determined the effects on cell internalization. We found that cells of distinct lineages depend on common actomyosin-based mechanisms to gastrulate, but different cell fate regulators, and, surprisingly, different cell polarity regulators. We conclude that diverse cell fate and cell polarity regulators control common mechanisms of morphogenesis in C. elegans. The results highlight the variety of developmental patterning mechanisms that can be associated with common cytoskeletal mechanisms in the morphogenesis of an animal embryo.     

Clonal analysis of <Emphasis Type="Italic">Distal-less</Emphasis> and <Emphasis Type="Italic">engrailed</Emphasis> expression patterns during early morphogenesis of uniramous and biramous crustacean limbs

In order to investigate the correlation of cell lineage, gene expression, and morphogenesis of uniramous and biramous limbs we studied limb formation in the thorax and pleon of the amphipod Orchestia cavimana and the isopod Porcellio scaber. We took advantage of the fact that in amphipod and isopod crustaceans—both Malacostraca—uniramous limbs evolved independently in the thorax whereas ancestral biramous limbs are formed in the pleon (abdomen). The gene Distal-less is expressed in the early limb buds as in other arthropods. Accordingly, it is likely to be responsible for the development of the proximodistal axis of the appendages. Double staining of Distal-less and Engrailed proteins suggests that Distal-less in the pleon of the amphipod Orchestia might not be under the control of the Wingless protein. Additionally, we studied axis formation of the uniramous and biramous limbs. In both species investigated, biramous limbs originate exclusively by the subdivision of the original limb bud. Both distal elements continuously express Distal-less. There is flexibility in the suppression of the development of additional branches in the crustacean limb. In the amphipod O. cavimana, uniramous thoracopods are formed by downregulation of Distal-less in the area where, in biramous limbs, the exopodites would occur. In contrast, this region never expresses Distal-less in the uniramous thoracopods of the isopod P. scaber. Our results suggest that the gene expression pattern is independent of the cell division pattern. Gene expression domains and morphogenesis of limbs and segments, on the other hand, show a good correlation.Edited by D. Tautz     

Immunocytochemical localization of serotonin in embryos, larvae and adults of the lancelet, Branchiostoma floridae

Serotonin (5-hydroxytryptamine) is a biogenic amine distributed throughout the metazoans and has an old evolutionary history. It is involved as a developmental signal in the early morphogenesis of both invertebrates and vertebrates, whereas in adults it acts mainly as a neurotransmitter and gastrointestinal hormone. In vertebrates, serotonin regulates the morphogenesis of the central nervous system and the specification of serotonergic as well as dopaminergic neurons. The present study uses, as an experimental model, an invertebrate chordate, the lancelet Branchiostoma floridae, characterized by its remarkable homologies with vertebrates that allows the 'bauplan' of the probable ancestor of vertebrates to be outlined. In particular, the involvement of serotonin as a developmental signal in embryos and larvae, as well as a neurotransmitter and gastrointestinal hormone in adult specimens of Branchiostoma floridae, gives further support to a common origin of cephalocordates and vertebrates.     

Epithelial morphogenesis.

The identification of protein factors, such as epimorphin, scatter factor, and activin, that induce epithelial branching and convergent extension-like movements in embryonic tissues are important breakthroughs in our understanding of the role of mesenchyme in epithelial morphogenesis. Moreover, the development of simple in vitro epithelial cell systems that undergo morphogenesis in response to these factors should provide a means to investigate the cellular and molecular bases of the morphogenetic movements themselves. Although many different cellular processes are involved in such morphogenetic behaviors, cell rearrangement is a particularly intriguing one that will be important to study further. Several considerations lead to the prediction that a dynamic regulation of cell-cell adhesion is likely to play a central role in cell rearrangements and epithelial morphogenesis. Ultimately, a greater issue to be addressed is how the different cellular mechanisms participating in epithelial morphogenesis are coordinated and regulated, so as to generate the diverse patterns found in various epithelia.     

Homologies of process and modular elements of embryonic construction

There are several signal transduction pathways that integrate embryonic development. We find that both within species and between species, these pathways constitute homologous modules. The processes, themselves, can be considered homologous, just as structures can be considered homologous. Just like vertebrate limbs, these pathways are composed of homologous parts (in this case, the proteins of the pathway) that are organized in homologous ways. These pathways are conserved through evolutionary time, and they undergo descent with modification. Such homologies of processes become critical to the discussion of evolution and development when we consider (1) that evolution depends on heritable changes in development, (2) that development is modular such that different modules can change without affecting other modules, (3) that modules can be co-opted into new functions, and (4) that modules depend on intercellular communication.     

THE PERIOD GENE OF THE GERMAN COCKROACH AND ITS NOVEL LINKING POWER BETWEEN VERTEBRATE AND INVERTEBRATE

Circadian clock protein PERIOD (PER) is essential for the endogenous clockworks in diverse lineages within Metazoa, but the protein sequences, the clock protein interactions, and the photic responses are variant and different between vertebrate and invertebrate PER homologs. Here we identified the German cockroach PER homologs and found it could bridge the huge phylogenetic gap and make possible a more precise protein sequence comparison between vertebrate and invertebrate PER homologs. Seven blocks of conserved regions (c1–c7) interspersed within PER proteins were defined, and two new significant homologies were found in the upstream portion of c3 region and in the c7 region, respectively. In addition, we found all dipteran insects PER homologs lack the c7 region and its following amino acid residues. Our results not only reveal the homology and divergence, but also imply the constraint and plasticity of divergent PER proteins during the course of evolution. These findings lay a solid foundation for understanding the general and divergent properties of circadian clockworks in diverse lineages within Metazoa.     

The period gene of the German cockroach and its novel linking power between vertebrate and invertebrate

Circadian clock protein PERIOD (PER) is essential for the endogenous clockworks in diverse lineages within Metazoa, but the protein sequences, the clock protein interactions, and the photic responses are variant and different between vertebrate and invertebrate PER homologs. Here we identified the German cockroach PER homologs and found it could bridge the huge phylogenetic gap and make possible a more precise protein sequence comparison between vertebrate and invertebrate PER homologs. Seven blocks of conserved regions (c1-c7) interspersed within PER proteins were defined, and two new significant homologies were found in the upstream portion of c3 region and in the c7 region, respectively. In addition, we found all dipteran insects PER homologs lack the c7 region and its following amino acid residues. Our results not only reveal the homology and divergence, but also imply the constraint and plasticity of divergent PER proteins during the course of evolution. These findings lay a solid foundation for understanding the general and divergent properties of circadian clockworks in diverse lineages within Metazoa.     

Appendage Homologies and the First Record of Eyes in Platycopid Ostracods, with the Description of a New Species of Keijcyoidea (Crustacea: Ostracoda) from Japan

A median nauplius eye is reported for the first time in a platycopid ostracod, a group hitherto considered to be blind. A new species of the platycopid ostracod genus Keijcyoidea is described from coastal rocky marine habitats on the Pacific coast of Japan. Observations of living specimens in the laboratory show that it is capable of burrowing to a depth of several millimeters in sandy sediment, using the first two head appendages (antennulae and antennae) and the furca. Females brooded a maximum of five eggs in the posterior brood space of the carapace. The homologies and phylogenetic implications of the trunk segmentation and limbs are discussed, paying particular attention to the sexually dimorphic fifth and sixth limbs; the copulatory appendages of both sexes are interpreted as being attached to trunk segments T6–T7 (counting from the posterior; T1 = posteriormost segment).     

Evolutionary conservation of microtubule-capture mechanisms

The dynamic nature of microtubules allows them to search the three-dimensional space of the cell. But what are they looking for? During cellular morphogenesis, microtubules are captured at sites just under the plasma membrane, and this polarizes the microtubule array and associated organelles. Recent data indicate that the signalling pathways that are involved in regulating the different microtubule cortical interactions are not only conserved between species, but also that they function in diverse processes.     

Homology of Holocene ostracode biramous appendages with those of other crustaceans: the protopod, epipod, exopod and endopod

Unambiguously biramous appendages with a proximal precoxa, well-defined coxa and basis, setose plate-like epipod originating on the precoxa, and both an endopod and exopod attached to the terminal end of the basis are described from several living Ostracoda of the order Halo-cyprida (Myodocopa). These limbs are proposed as the best choice for comparison of ostracode limbs with those of other crustaceans and fossil arthropods with preserved limbs, such as the Cambrian superficially ostracode-like Kunmingella and Hesslandona. The 2nd maxilla of Metapolycope (Cladocopina) and 1st trunk limb of Spelaeoecia, Deeveya and Thaumatoconcha (all Halocypridina) are illustrated, and clear homologies are shown between the parts of these limbs and those of some general crustacean models as well as some of the remarkable crustacean s.s. Orsten fossils. No living ostracodes exhibit only primitive morphology; all have at least some (usually many) derived characters. Few have the probably primitive attribute of trunk segmentation (two genera of halocyprid Myodocopa, one order plus one genus of Podocopa, and the problematic Manawa); unambiguously biramous limbs are limited to a few halo-cyprids. Homologies between podocopid limbs and those of the illustrated primitive myodocopid limbs are tentatively suggested. A setose plate-like extension, often attached basally to a podocopid protopod, is probably homologous to the myodocopid epipod, which was present at least as early as the Triassic. Somewhat more distal, less setose, and plate-like extensions, present on some podocopid limbs (e.g., mandible), may be homologous instead to the exopod (clearly present on myodocopid mandibles). The coxa (or precoxa) is by definition the most basal part of the limb. A molar-like tooth is present proximally on the mandibular protopod of many ostracodes; it is the coxal endite and projects medially from the coxa (or proximal protopod). The Ostracoda is probably a monophyletic crustacean group composed of Myodocopa and Podocopa. All have a unique juvenile (not a larva) initially with three or more limbs. Except that juveniles lack some setae and limbs, they are morphologially similar to the adult. Thus the following suite of characters in all instars may be considered a synapomorphy uniting all Ostracoda: (1) Each pair of limbs is uniquely different from the others. (2) The whole body is completely enclosed within a bivalved carapace that lacks growth lines. (3) No more than nine pairs of limbs are present in any instar. (4) The body shows little or no segmentation, with no more than ten dorsally defined trunk segments. No other crustaceans have this suite of characters. A probable synapomorphy uniting the Podocopa is a 2nd antenna with exopod reduced relative to the endopod.