Myriapod metamerism and arthropod segmentation

Outstanding progress in understanding segmentation of tracheate arthropods (Atelocerata), i.e. Chilopoda, Diplopoda, Pauropoda, Symphyla and Insecta, has been gained through experimental studies carried out on a single, very derivative organism, i.e. Drosophila. We stress the need for a broader comparative approach. We have studied the segmental structure of the trunk in geophilomorph centipedes, where we can identify morphogenetic units of two, four, eight or 16 segments. Accordingly, we sketch an improved model for arthropod segmentation, with the following initial steps: (a) biochemical marking of a very few repetitive units (eosegments); (b) iterative duplications of this first periodicity, until the embryo acquires an array of biochemical markings matching the whole number of segments of the future larva or juvenile specimen; (c) transpatterning, stabilization and interpretation of this 'segmental' arrangement; (d) possible repatterning, to give a final repetitive pattern we define as metasegmental. Finally, we express some doubt about the homology between annelid and arthropod segmentation.     

How does arthropod segment number evolve?—some clues from centipedes

Summary Studies of intraspecific variation in the number of trunk segments of geophilomorph centipedes provide clues as to how different species of arthropods, and whole clades in some cases, come to be characterized by different segment numbers. However, although previous work in this area has revealed an interesting geographical pattern—a latitudinal cline in which segment number decreases with increasing latitude—the causality of the cline remains obscure. Is it because of selection on genetically based variation, or is it a result of a form of phenotypic plasticity in which the segmentation process is directly affected by a latitude‐correlated factor such as temperature? Here, we provide some indirect evidence for plasticity. If the cline is indeed a plastic one, a paradox arises, because the cline mirrors interspecific variation—geophilomorph species with more northern ranges typically have fewer segments than those from further south—but interspecific differences cannot arise from nonheritable variation. We propose a resolution of this apparent paradox via a model in which genetic and environmental factors interact through selection acting on developmental reaction norms.     

The sternal pore areas of geophilomorph centipedes (Chilopoda: Geophilomorpha)

Most geophilomorph centipedes have segmental clusters of exocrine glands whose opening pores are arranged in more or less well-defined sternal pore areas. We describe here the cuticular structures forming and/or accompanying the gland openings on the sternites and the shape of the pore areas along the body axis in representatives of most geophilomorph families. The cuticular ring around the pore may exhibit either of two forms. In Himantariidae ( Himantarium ) and in Dignathodontidae ( Henia ) the ring looks like a continuous ribbon with a visible suture, whereas in the representatives of the remaining families no suture is seen. As to the distribution of the pores on ventral surface of the body, we record the presence of pores on the last leg-bearing segment of Clinopodes flavidus , whereas that segment was described as poreless in all geophilomorphs. We also provide a taxonomic survey of shape and distribution of pore areas in the individual families, where the pore areas may take very different shapes that we regard as transformational homologues. As for the segmental distribution of sternal pore areas, there is a considerable amount of complexity along the trunk of geophilomorph centipedes, in contrast to the apparently uniform trunk structure.     

Segment number,body length,and latitude in geophilomorph centipedes: a ‘converse‐Bergmann’ pattern

There is a negative relationship between trunk segment number and latitude among geophilomorph centipedes in general. A similar relationship is known to exist within the most intensively‐studied geophilomorph species, Strigamia maritima, and also within several other species from this group. Previously, it was considered that this relationship did not involve body length; instead, individuals of S. maritima with more segments were considered to be more finely subdivided (not longer) than those with fewer segments. This incorrect interpretation arose from the difficulty of reliably separating post‐embryonic stages and thus of making a simple and direct comparison. In the present study, we build on recent work that facilitates such comparisons; and we show conclusively that individuals with more segments are longer. Our finding means that it is now possible to connect the work on S. maritima in particular, and on geophilomorph centipedes in general, with the debate about Bergmann's ‘rule’: the proposal that body size increases with increasing latitude. There is a clear ‘converse‐Bergmann’ pattern, as has been found in several other taxa. We propose an adaptive hypothesis that may explain why geophilomorphs show this pattern. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ?? , ??–??.     

The evolution of segmentation of centipede trunk and appendages

The segmentation of centipedes is interpreted in the light of a biphasic model of segmentation (holomeric plus meromeric). The mid-body anomaly (e.g. in the alternating short and long terga, or in the sequence of segments with and without spiracles) is regarded as due to an early patterning of the embryo, occurring before the onset of meromeric segmentation and affecting a level within the fourth eosegment of the trunk. Comparisons with the Diplopoda suggest that genital structures such as millipede gonopods did probably develop originally at this spot, whose position remained marked even after the transition from a putatively progoneate to the current opisthogoneate condition of centipedes, perhaps following gene duplication and divergence of expression patterns of the paralogues. A new lower limit for the number of leg-bearing segments [27, in a male specimen of Schendylops oligopus (Pereira, Minelli & Barbieri,1995)] is established for Geophilomorpha. Coevolutionary trends involving the segmentation of the trunk, the segmentation of the appendages (especially the antennae), the postembryonic developmental schedule and the presence or absence of regeneration ability supports a recent view of the appendages as evolutionarily divergent duplicates of the main body axis.     

A double segment periodicity underlies segment generation in centipede development

The number of leg-bearing segments in centipedes varies extensively, between 15 and 191, and yet it is always odd. This suggests that segment generation in centipedes involves a stage with double segment periodicity and that evolutionary variation in segment number reflects the generation of these double segmental units. However, previous studies have revealed no trace of this. Here we report the expression of two genes, an odd-skipped related gene (odr1) and a caudal homolog, that serve as markers for early steps of segment formation in the geophilomorph centipede, Strigamia maritima. Dynamic expression of odr1 around the proctodaeum resolves into a series of concentric rings, revealing a pattern of double segment periodicity in overtly unsegmented tissue. Initially, the expression of the caudal homolog mirrors this double segment periodicity, but shortly before engrailed expression and overt segmentation, the intercalation of additional stripes generates a repeat with single segment periodicity. Our results provide the first clues about the causality of the unique and fascinating "all-odd" pattern of variation in centipede segment numbers and have implications for the evolution of the mechanisms of arthropod segmentation.     

Variation in body segment number within and between populations of the centipede Strigamia maritima (Chilopoda: Geophilomorpha)

Although most arthropod species have a fixed number of body segments, one order of centipedes – the Geophilomorpha – provides an unusual opportunity to study the variation and microevolution of segment number. This is because all species in all but one family exhibit variation in the number of leg‐bearing segments (LBS) within and between natural populations. One species in particular, the coastal geophilomorph Strigamia maritima, has become a ‘model system’ for these studies, because of its high population densities and the consequent ease of collecting large samples. Previous studies on this species have examined various aspects of segment number variation. However, most studies have characterized each population by an LBS distribution and a mean LBS number that are based on data from all life‐stages. Here, we dissect the variation within as well as between populations and show that different cohorts within a population often have significantly different LBS number distributions. This is almost certainly due to developmental plasticity, probably related to the prevailing microhabitat temperature within brood chambers, but possibly related to other environmental factors too. Although we found no evidence of selection, the fact that different species of geophilomorphs have different LBS distributions suggests that, in the long term, selection may act on the developmental reaction norm of LBS number. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 678–685.     

Segmentation of the millipede trunk as suggested by a homeotic mutant with six extra pairs of gonopods

Background

The mismatch between dorsal and ventral trunk features along the millipede trunk was long a subject of controversy, largely resting on alternative interpretations of segmentation. Most models of arthropod segmentation presuppose a strict sequential antero-posterior specification of trunk segments, whereas alternative models involve the early delineation of a limited number of ‘primary segments’ followed by their sequential stereotypic subdivision into 2ⁿ definitive segments. The ‘primary segments’ should be intended as units identified by molecular markers, rather than as overt morphological entities. Two predictions were suggested to test the plausibility of multiple-duplication models of segmentation: first, a specific pattern of evolvability of segment number in those arthropod clades in which segment number is not fixed (e.g., epimorphic centipedes and millipedes); second, the occurrence of discrete multisegmental patterns due to early, initially contiguous positional markers.

Results

We describe a unique case of a homeotic millipede with 6 extra pairs of ectopic gonopods replacing walking legs on rings 8 (leg-pairs 10-11), 15 (leg-pairs 24-25) and 16 (leg-pairs 26-27); we discuss the segmental distribution of these appendages in the framework of alternative models of segmentation and present an interpretation of the origin of the distribution of the additional gonopods. The anterior set of contiguous gonopods (those normally occurring on ring 7 plus the first set of ectopic ones on ring 8) is reiterated by the posterior set (on rings 15-16) after exactly 16 leg positions along the AP body axis. This suggests that a body section including 16 leg pairs could be a module deriving from 4 cycles of regular binary splitting of an embryonic ‘primary segment’.

Conclusions

A very likely early determination of the sites of the future metamorphosis of walking legs into gonopods and a segmentation process according to the multiplicative model may provide a detailed explanation for the distribution of the extra gonopods in the homeotic specimen. The hypothesized steps of segmentation are similar in both a normal and the studied homeotic specimen. The difference between them would consist in the size of the embryonic trunk region endowed with a positional marker whose presence will later determine the replacement of walking legs by gonopods.     

Variable segment number in centipedes: population genetics meets evolutionary developmental biology

The case studies of population genetics focus on intraspecific variation, but most cases--at least where the variation is polymorphic--deal with characters that are not directly linked to organismic structure or ontogeny. Conversely, the case studies of evolutionary developmental biology focus directly on structure/ontogeny, but usually involve only interspecific comparisons. To integrate these complementary approaches, it is desirable to have a model system that permits study of intraspecific variation in development, using a character whose genetic basis either is already known or can be elucidated. Segment number in geophilomorph centipedes is proposed as a possible model system of this kind. Segment number is variable in natural populations of geophilomorphs, while in the other centipede orders it is fixed, either completely (scutigeromorphs, lithobiomorphs), or at least within species (scolopendromorphs). Statistical analysis of data on the extent of variation in different geophilomorph species suggests that segment number may be of selective importance, rather than the variation being merely an inevitable consequence of the difficulty of achieving a high degree of repeatability when there is a large number of segments.     

Arthropod segmentation: why centipedes are odd

Recent work has revealed a double segmental periodicity of gene expression in the centipede, a potential molecular explanation for the observation that this arthropod always has an odd number of trunk segments. Is this an oddity of centipedes, or might it mean that double segmental pair-rule patterning dates back to the Ur-arthropod?     

An early temperature‐sensitive period for the plasticity of segment number in the centipede Strigamia maritima

Geophilomorph centipedes show variation in segment number (a) between closely related species and (b) within and between populations of the same species. We have previously shown for a Scottish population of the coastal centipede Strigamia maritima that the temperature of embryonic development is one of the factors that affects the segment number of hatchlings, and hence of adults, as these animals grow epimorphically—that is, without postembryonic addition of segments. Here, we show, using temperature‐shift experiments, that the main developmental period during which embryos are sensitive to environmental temperature is surprisingly early, during blastoderm formation and before, or very shortly after, the onset of segmentation.     

Population Genetic Structure of a Centipede Species with High Levels of Developmental Instability

European populations of the geophilomorph centipede Haplophilus subterraneus show a high proportion of individuals with morphological anomalies, suggesting high levels of developmental instability. The broad geographic distribution of this phenomenon seems to exclude local environmental causes, but the source of instability is still to be identified. The goal of the present study was to collect quantitative data on the occurrence of phenodeviants in different populations, along with data on the patterns of genetic variation within and between populations, in order to investigate possible association between developmental instability and genetic features. In a sample of 11 populations of H. subterraneus, distributed in western and central Europe, we looked for phenodeviants, in particular with respect to trunk morphology, and studied genetic variation through the genotyping of microsatellite loci. Overall, no support was found to the idea that developmental instability in H. subterraneus is related to a specific patterns of genetic variation, including inbreeding estimates. We identified a major genetic partition that subdivides French populations from the others, and a low divergence among northwestern areas, which are possibly related to the post-glacial recolonization from southern refugia and/or to recent anthropogenic soil displacements. A weak correlation between individual number of leg bearing segments and the occurrence of trunk anomalies seems to support a trade-off between these two developmental traits. These results, complemented by preliminary data on developmental stability in two related species, suggest that the phenomenon has not a simple taxonomic distribution, while it exhibits an apparent localization in central and eastern Europe.     

Latitudinal cline in segment number in an arthropod species, Strigamia maritima

Arthropods vary more than 30-fold in segment number. The evolutionary origins of differences in segment number among species must ultimately lie in intraspecific variation. Yet paradoxically, in most groups of arthropods, the number of segments is fixed for each species and shows no intra- or interpopulation variation at all. Geophilomorph centipedes are an exception to this general rule, and exhibit intraspecific variation in segment number, with differences between individuals being determined during embryonic development and hence independent of population age structure. Significant differences in segment number between different geographical populations of the same species have been previously reported, but insufficient sampling has been conducted to reveal any particular geographical pattern. Here, we reveal a latitudinal cline in segment number in the geophilomorph species Strigamia maritima: segment number in British populations decreases with distance north. This is the first such cline to be reported for any centipede species; indeed as far as we are aware it is the first such cline reported for any arthropod species. In vertebrates, fish are known to exhibit a latitudinal cline in segment number, but interestingly, this is in the opposite direction; fish add segments with increasing latitude, centipedes subtract them.     

Evolutionary trends and patterns in centipede segment number based on a cladistic analysis of Mecistocephalidae (Chilopoda: Geophilomorpha)

Abstract.  Evolutionary changes in segment number during the radiation of Mecistocephalidae, a group of geophilomorph centipedes with segment number usually invariant at the species level, were explored based on a cladistic analysis of forty-six mecistocephalid species, representative of the extant diversity in segment number. The data matrix included 118 morphological characters. Trends were recognized in the evolution of segment number and discussed in relation to the underlying ontogenetic mechanisms of segmentation. The basic trend was towards an increasingly higher number of leg-bearing segments, from (most probably) forty-one to sixty-five (101 in one exceptional case). Changes always involved even sets of segments. Additions of two, four or eight segments usually occurred, but a case of overall duplication of the whole number was also documented. Most changes occurred starting from values belonging to the arithmetical series forty-one, forty-five, forty-nine, whereas the intermediate values forty-three, forty-seven, fifty-one were often evolutionary dead-ends. This evidence suggests a multiplicative mechanism of segmentation involving one or more final run of duplication, as well as a precise control of the final number of segments which produces absolute number stability, except for a single, highly derived species with an exceptionally high number of segments. These ideas contribute to a more general model of arthropod segmentation recently developed by Minelli. A taxonomic revision of mecistocephalids is presented: three subfamilies are proposed (Arrupinae, Dicellophilinae and Mecistocephalinae) and Sundarrup is recognized as a junior synonym of Anarrup .     

Hox gene sequences from the geophilomorph centipede Pachymerium ferrugineum (C. L. Koch, 1835) (Chilopoda: Geophilomorpha: Geophilidae): implications for the evolution of the Hox class genes of arthropods.

Here we report on a partial screen for Hox gene sequences from the geophilomorph centipede Pachymerium ferrugineum, resulting in 11 different sequences. All of these sequences could be homologized to specific Drosophila genes, yielding two representatives for the Dfd class and one each for the remaining classes. Phylogenetic analysis of these data with a broad sample of arthropod/onychophoran homologous sequences confirmed these results and provided further support for the monophyly of the Hox3/zen class. Conversely, the phylogenetic status of ftz-type genes remains uncertain. Our results complement the previous partial findings for two other centipedes (the scolopendromorph Ethmostigmus rubripes and the lithobiomorph Lithobius forficatus) and confirm the expectation that in myriapods, too, all Hox genes classes are present. This suggests that even the Chilopoda, with uniform trunk segments, have the same number of Hox genes as the more tagmatized Insecta.     

Pincer-like claws in centipedes (Chilopoda): multiple evolutionary origin of similar form and serial pattern

In most Chilopoda, the walking legs end in a single-tip claw usually accompanied by short accessory spines. Instead, in all species of three small and only distantly related geophilomorph taxa (Diphyonyx, Neogeophilidae, Eucratonyx), the claws of an anterior set of leg pairs are unusually pincer-like. By integrating different microscopic techniques, including confocal laser scanning microscopy, we found that these modified claws are very similar in form, internal structure, and pattern of variation in shape along the trunk in all three taxa: the claws are distinctly swollen and bent, provided with peculiar bulges, and flanked by a conspicuous additional branch, either cylindrical or flattened, which overreaches the tip of the claw; instead, the internal cuticular features are not modified with respect to the condition in the other centipedes, claiming against the possibility of controlled abduction/adduction between claw and branch. Irrespective of the total number of leg pairs (63–129), the claws change gradually from pincer-like to usual shape invariantly in the range spanning between the 34 and the 45% of the total number of leg pairs. Despite these similarities, pincer-like claws originated independently in the three taxa, and by way of fundamentally different changes, either by the dramatic modification of the already existent anterior accessory spine (Diphyonyx, Neogeophilidae) or by the production of a novel cuticular projection (Eucratonyx). Moreover, their shared pattern of variation along the body was most probably constrained by already operating developmental processes controlling the longitudinal patterning of the trunk.     

Expression of hunchback during trunk segmentation in the branchiopod crustacean Artemia franciscana

Comparative studies have shown that some aspects of segmentation are widely conserved among arthropods. Yet, it is still unclear whether the molecular prepatterns that are required for segmentation in Drosophila are likely to be similarly conserved in other arthropod groups. Homologues of the Drosophila gap genes, like hunchback, show regionally restricted expression patterns during the early phases of segmentation in diverse insects, but their expression patterns in other arthropod groups are not yet known. Here, we report the cloning of a hunchback orthologue from the crustacean Artemia franciscana and its expression during the formation of trunk segments. Artemia hunchback is expressed in a series of segmental stripes that correspond to individual thoracic/trunk, genital, and postgenital segments. However, this expression is not associated with the segmenting ectoderm but is restricted to mesodermal cells that associate with the ectoderm in a regular metameric pattern. All cells in the early segmental mesoderm appear to express hunchback. Later, mesodermal expression fades, and a complex expression pattern appears in the central nervous system (CNS), which is comparable to hunchback expression in the CNS of insects. No regionally restricted expression, reminiscent of gap gene expression, is observed during trunk segmentation. These patterns suggest that the expression patterns of hunchback in the mesoderm and in the CNS are likely to be ancient and conserved among crustaceans and insects. In contrast, we find no evidence for a conserved role of hunchback in axial patterning in the trunk ectoderm.     

The evolution of centipede venom claws – Open questions and possible answers

The maxilliped venom claw is an intriguing structure in centipedes. We address open questions concerning this structure. The maxillipeds of fossil centipedes from the Carboniferous (about 300 million years old) have been described, but not been depicted previously. Re-investigation demonstrates that they resemble their modern counterparts. A Jurassic geophilomorph centipede (about 150 million years old) was originally described as possessing a rather leg-like maxilliped. Our re-investigation shows that the maxilliped is, in fact, highly specialized as in modern Geophilomorpha. A scenario for the evolution of the centipede maxilliped is presented. It supports one of the two supposed hypotheses of centipede phylogeny, the Pleurostigmophora hypothesis. Although this hypothesis appears now well established, many aspects of character evolution resulting from this phylogeny remain to be told in detail. One such aspect is the special joint of the maxilliped in some species of Cryptops. Cryptops is an in-group of Scolopendromorpha, but its maxilliped joint can resemble that of Lithobiomorpha or even possess a mixture of characters between the both. Detailed investigation of fossils, larger sample sizes of extant species, and developmental data will be necessary to allow further improvements of the reconstruction of the evolutionary history of centipedes.