Gerhard Scholtz

Phylogenetic systematics of the reptantian Decapoda (Crustacea, Malacostraca)

Although the biology of the reptantian Decapoda has been much studied, the last comprehensive review of reptantian systematics was published more than 80 years ago. We have used cladistic methods to reconstruct the phylogenetic system of the reptantian Decapoda. We can show that the Reptantia represent a monophyletic taxon. The classical groups, the ‘Palinura’, ‘Astacura’ and ‘Anomura’ are paraphyletic assemblages. The Polychelida is the sister-group of all other reptantians. The Astacida is not closely related to the Homarida, but is part of a large monophyletic taxon which also includes the Thalassinida, Anomala and Brachyura. The Anomala and Brachyura are sister-groups and the Thalassinida is the sister-group of both of them. Based on our reconstruction of the sister-group relationships within the Reptantia, we discuss alternative hypotheses of reptantian interrelationships, the systematic position of the Reptantia within the decapods, and draw some conclusions concerning the habits and appearance of the reptantian stem species.

The evolution of arthropod heads: reconciling morphological, developmental and palaeontological evidence.

Understanding the head is one of the great challenges in the fields of comparative anatomy, developmental biology, and palaeontology of arthropods. Numerous conflicting views and interpretations are based on an enormous variety of descriptive and experimental approaches. The interpretation of the head influences views on phylogenetic relationships within the Arthropoda as well as outgroup relationships. Here, we review current hypotheses about head segmentation and the nature of head structures from various perspectives, which we try to combine to gain a deeper understanding of the arthropod head. Though discussion about arthropod heads shows some progress, unquestioned concepts (e.g., a presegmental acron) are still a source of bias. Several interpretations are no longer tenable based on recent results from comparative molecular developmental studies, improved morphological investigations, and new fossils. Current data indicate that the anterior arthropod head comprises three elements: the protocerebral/ocular region, the deutocerebral/antennal/cheliceral segment, and the tritocerebral/pedipalpal/second antennal/intercalary segment. The labrum and the mouth are part of the protocerebral/ocular region. Whether the labrum derives from a former pair of limbs remains an open question, but a majority of data support its broad homology across the Euarthropoda. From the alignment of head segments between onychophorans and euarthropods, we develop the concept of “primary” and “secondary antennae” in Recent and fossil arthropods, posit that “primary antennae” are retained in some fossil euarthropods below the crown group level, and propose that Trilobita are stem lineage representatives of the Mandibulata.

The Articulata hypothesis – or what is a segment?

The long held view that annelids and arthropods are closely related (Articulata) has been challenged recently by phylogenetic analyses using molecular data. The outcome of these studies is a clade of moulting animals (Ecdysozoa) comprising arthropods and some taxa of the nemathelminth worms. Monophyly of the Ecdysozoa has not yet been shown convincingly on morphological evidence, but is strongly supported by molecular data. The implication of the Ecdysozoa hypothesis is that the type of segmentation found in annelids and arthropods must be either convergent or an ancestral feature of protostomes or even bilaterians. The present review discusses aspects of segmentation in annelids and arthropods at the genetic, cellular, morphogenetic and morphological levels. Based on numerous similarities not shared with other bilaterian taxa it is suggested that segmentation of annelids and arthropods is homologous and apomorphic for a monophyletic Articulata. However, the challenge provided by the molecular analyses should stimulate research programmes gaining more data such as on additional genes, cleavage patterns, molecular developmental biology, and the comparison of nervous systems at the level of single neurons.

Cleavage, germ band formation and head segmentation: the ground pattern of the Euarthropoda

Comparative embryological studies have always played an important role in the interpretation and understanding of arthropod origins and phylogeny (Bowler, 1994). Embryonic data have been used to support both arthropod monophyly (Weygoldt, 1979, 1986) as well as polyphyly (Anderson, 1973). Now there is convincing and increasing evidence from palaeontological, embryological, morphological, and molecular studies that arthropods are monophyletic (Weygoldt, 1986; Wagele, 1993; Walossek, 1993; Wheeler et al., 1993; Friedrich and Tautz, 1995; Wills et al., 1995; Wagele and Stanjek, 1995; Garey et al., 1996). This is especially clear for the ‘true’ arthropods, the Euarthropoda, which include the chelicerates, crustaceans, myriapods, and insects. The method of phylogenetic systematics (Hennig, 1950, 1966) allows not only the analysis of the phylogenetic relationships between taxa but it also offers a tool for the reconstruction of the ground pattern of a given monophyletic group (Ax, 1987).

Conserved and Convergent Organization in the Optic Lobes of Insects and Isopods, with Reference to Other Crustacean Taxa

The shared organization of three optic lobe neuropils—the lamina, medulla, and lobula—linked by chiasmata has been used to support arguments that insects and malacostracans are sister groups. However, in certain insects, the lobula is accompanied by a tectum‐like fourth neuropil, the lobula plate, characterized by wide‐field tangential neurons and linked to the medulla by uncrossed axons. The identification of a lobula plate in an isopod crustacean raises the question of whether the lobula plate of insects and isopods evolved convergently or are derived from a common ancestor. This question is here investigated by comparisons of insect and crustacean optic lobes. The basal branchiopod crustacean Triops has only two visual neuropils and no optic chiasma. This finding contrasts with the phyllocarid Nebalia pugettensis, a basal malacostracan whose lamina is linked by a chiasma to a medulla that is linked by a second chiasma to a retinotopic outswelling of the lateral protocerebrum, called the protolobula. In Nebalia, uncrossed axons from the medulla supply a minute fourth optic neuropil. Eumalacostracan crustaceans also possess two deep neuropils, one receiving crossed axons, the other uncrossed axons. However, in primitive insects, there is no separate fourth optic neuropil. Malacostracans and insects also differ in that the insect medulla comprises two nested neuropils separated by a layer of axons, called the Cuccati bundle. Comparisons suggest that neuroarchitectures of the lamina and medulla distal to the Cuccati bundle are equivalent to the eumalacostracan lamina and entire medulla. The occurrence of a second optic chiasma and protolobula are suggested to be synapomorphic for a malacostracan/insect clade. J. Comp. Neurol. 467:150–172, 2003.

The parthenogenetic Marmorkrebs (marbled crayfish) produces genetically uniform offspring

Genetically identical animals are very much in demand as laboratory objects because they allow conclusions about environmental and epigenetic effects on development, structures, and behavior. Furthermore, questions about the relative fitness of various genotypes can be addressed. However, genetically identical animals are relatively rare, in particular, organisms that combine a high reproduction rate and a complex organization. Based on its exclusively parthenogenetic reproduction mode, it has been suggested that the Marmorkrebs (Crustacea, Decapoda, Astacida), a recently discovered crayfish, is an excellent candidate for research addressing the aforementioned questions. However, until now, a study using molecular markers that clearly proves the genetic uniformity of the offspring has been lacking. Here, with this first molecular study, we show that this crayfish indeed produces genetically uniform clones. We tested this with 19 related individuals of various generations of a Marmorkrebs population by means of six different microsatellite markers. We found that all examined specimens were identical in their allelic composition. Furthermore, half of the analyzed loci were heterozygous. These results and the absence of meioses in previous histological studies of the ovaries lead us to conclude the Marmorkrebs propagates apomictically. Thus, a genetically uniform organism with complex morphology, development, and behavior is now available for various laboratory studies.

Phylogenetic relationships within the Phyllopoda (Crustacea, Branchiopoda) based on mitochondrial and nuclear markers.

For several decades the relationships within the Branchiopoda (Anostraca + Phyllopoda) have been a matter of controversy. Interpretations of plesiomorphic or apomorphic character states are a difficult venture, in particular in the Phyllopoda. We explore the relationships within the Phyllopoda at the level of nucleotid comparisons of the two genes 12S rDNA (mitochondrial) and EF1alpha (nuclear), and at a higher molecular level based on introns found in the gene EF1alpha. Within the Phyllopoda our explorations show further evidence for a non-monophyletic Conchostraca (Spinicaudata + Cyclestherida + Laevicaudata). The monotypic Cyclestherida is more closely related to the Cladocera, both together forming the Cladoceromorpha. The Spinicaudata (Leptestheriidae, Limnadiidae, and Cyzicidae) is well supported. Spinicaudata and Cladoceromorpha form a monophylum. The position of the Laevicaudata remains unclear but we find neither support for a sister group relationship to the Spinicaudata nor for a close relationship of Laevicaudata and Cladocera. Within the Cladocera, we favour the Gymnomera concept with the monotypic Haplopoda being the sister group to the monophyletic Onychopoda. The Ctenopoda seems to be the sister group to the Gymnomera, which contradicts the common view of a more basal position of the Ctenopoda.

Filling the gap between identified neuroblasts and neurons in crustaceans adds new support for Tetraconata

The complex spatio-temporal patterns of development and anatomy of nervous systems play a key role in our understanding of arthropod evolution. However, the degree of resolution of neural processes is not always detailed enough to claim homology between arthropod groups. One example is neural precursors and their progeny in crustaceans and insects. Pioneer neurons of crustaceans and insects show some similarities that indicate homology. In contrast, the differentiation of insect and crustacean neuroblasts (NBs) shows profound differences and their homology is controversial. For Drosophila and grasshoppers, the complete lineage of several NBs up to formation of pioneer neurons is known. Apart from data on median NBs no comparable results exist for Crustacea. Accordingly, it is not clear where the crustacean pioneer neurons come from and whether there are NBs lateral to the midline homologous to those of insects. To fill this gap, individual NBs in the ventral neuroectoderm of the crustacean Orchestia cavimana were labelled in vivo with a fluorescent dye. A partial neuroblast map was established and for the first time lineages from individual NBs to identified pioneer neurons were established in a crustacean. Our data strongly suggest homology of NBs and their lineages, providing further evidence for a close insect–crustacean relationship.

Mitogenomic analysis of decapod crustacean phylogeny corroborates traditional views on their relationships

Phylogenetic relationships within decapod crustaceans are highly controversial. Even recent analyses based on molecular datasets have shown largely contradictory results. Previous studies using mitochondrial genomes are promising but suffer from a poor and unbalanced taxon sampling. To fill these gaps we sequenced the (nearly) complete mitochondrial genomes of 13 decapod species: Stenopus hispidus, Polycheles typhlops, Panulirus versicolor, Scyllarides latus, Enoplometopus occidentalis, Homarus gammarus, Procambarus fallax f. virginalis, Upogebia major, Neaxius acanthus, Calocaris macandreae, Corallianassa coutierei, Cryptolithodes sitchensis, Neopetrolisthes maculatus, and add that of Dromia personata. Our new data allow for comprehensive analyses of decapod phylogeny using the mitochondrial genomes of 50 species covering all major taxa of the Decapoda. Five species of Stomatopoda and one species of Euphausiacea serve as outgroups. Most of our analyses using Maximum Likelihood (ML) and Bayesian inference (BI) of nucleotide and amino acid datasets revealed congruent topologies for higher level decapod relationships: (((((((Anomala, Brachyura), Thalassinida: Gebiidea), Thalassinida: Axiidea), (Astacidea, Polychelida), Achelata), Stenopodidea), Caridea), Dendrobranchiata). This result corroborates several traditional morphological views and adds new perspectives. In particular, the position of Polychelida is surprising. Nevertheless, some problems can be identified. In a minority of analyses the basal branching of Reptantia is not fully resolved, Thalassinida are monophyletic; Polychelida are the sister group to Achelata, and Stenopodidea are resolved as sister group to Caridea. Despite this and although some nodal supports are low in our phylogenetic trees, we think that the largely stable topology of the trees regardless of different types of analyses suggests that mitochondrial genomes show good potential to resolve the relationship within Decapoda.

The chelifores of sea spiders (Arthropoda, Pycnogonida) are the appendages of the deutocerebral segment.

SUMMARY Within the last decade, gene expression patterns and neuro‐anatomical data have led to a new consensus concerning the long‐debated association between anterior limbs and neuromeres in the arthropod head. According to this new view, the first appendage in all extant euarthropods is innervated by the second neuromere, the deutocerebrum, whereas the anterior‐most head region bearing the protocerebrum lacks an appendage. This stands in contrast to the clearly protocerebrally targeted “antennae” of Onychophora and to some evidence for protocerebral limbs in fossil euarthropod representatives. Yet, the latter “frontal appendages” or “primary antennae” have most likely been reduced or lost in the lineage, leading to extant taxa. Surprisingly, a recent neuro‐anatomical study on a pycnogonid challenged this evolutionary scenario, reporting a protocerebral innervation of the first appendages, the chelifores. However, this interpretation was soon after questioned by Hox gene expression data. To re‐evaluate the unresolved controversy, we analyzed neuro‐anatomy and neurogenesis in four pycnogonid species using immunohistochemical techniques. We clearly show the postprotocerebral innervation of the chelifores, which is resolved as the plesiomorphic condition in pycnogonids when evaluated against a recently published comprehensive phylogeny. By providing direct morphological support for the deutocerebral status of the cheliforal ganglia, we reconcile morphological and gene expression data and argue for a corresponding position between the anterior‐most appendages in all extant euarthropods. Consequently, other structures have to be scrutinized to illuminate the fate of a presumptive protocerebral appendage in recent euarthropods. The labrum and the “frontal filaments” of some crustaceans are possible candidates for this approach.