Temperature-dependent plasticity of segment number in an arthropod species: the centipede Strigamia maritima

SUMMARY The evolution of arthropod segment number provides us with a paradox, because, whereas there is more than 20‐fold variation in this character overall, most classes and orders of arthropods are composed of species that lack any variation in the number of segments. So, what is the origin of the higher‐level variation? The centipede order Geophilomorpha is unusual because, with the exception of one of its families, all species exhibit intraspecific variation in segment number. Hence it provides an opportunity to investigate how segment number may change in a microevolutionary context. Here, we show that segment number can be directly altered by an environmental factor (temperature)—this is the first such demonstration for any arthropod. The direction of the effect is such that higher temperature during embryogenesis produces more segments. This potentially explains an intraspecific cline in the species concerned, Strigamia maritima, but it does not explain how such a cline is translated into the parallel interspecific pattern of lower‐latitude species having more segments. Given the plastic nature of the intraspecific variation, its link with interspecific differences may lie in selection acting on developmental reaction norms.     

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 .     

Demonstration of a heritable component of the variation in segment number in the centipede Strigamia maritima

SUMMARY Here we address the question of how arthropod segment number may evolve by reporting the results of further work on the model system Strigamia maritima . Recently, we showed that there was a plastic component of the variation in segment number within this species; now we demonstrate that there is also a heritable component. This is important because it enables a connection to be made between the known latitudinal trend among species of geophilomorph centipedes (more segments at lower latitudes) and the parallel trend within them. This latter trend is best documented in S. maritima but is also known in several other species. However, while a general connection between the inter- and intraspecific trends can now be made, deciding upon a specific hypothesis of the nature of the selection involved is still problematic. We provide two alternative hypotheses, one based on the temperature-related plasticity in segment number being adaptive, the other based on it being nonadaptive.     

Morphology and diversity of the forcipules in Strigamia centipedes (Chilopoda,Geophilomorpha)

The morphology of the venomous limbs (forcipules) of 13 species of Strigamia and of six other geophilomorphs was studied with light microscopy, scanning electron microscopy, and, for a subsample, with confocal laser scanning microscopy. In all Strigamia species a well-distinct denticle is present invariantly on the inner side of the terminal article (tarsungulum), in sub-basal position, just proximal to a faint transverse sulcus and a cuticular introflexion that corresponds to the insertion point of a tendon. Strigamia species differ mainly in size and shape of the denticle and thickness of the distal part of the tarsungulum, suggesting some functional diversity in piercing and handling prey. Anatomical evidence supports the hypothesis that the tarsungulum corresponds to two ancestral articles and a denticle at the basis of the tarsungulum originated multiple times within geophilomorphs, however in different positions corresponding to either the ancestral sub-terminal article (in Strigamia, other Geophiloidea and some Schendylidae) or the ancestral terminal article (in the himantariid Thracophilus).     

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.     

A new miniature species of geophilomorph centipede from the Ecuadorian Amazon rainforest (Chilopoda: Geophilomorpha: Ballophilidae)

A new miniature species of geophilomorph centipede, Ityphilus grismadoi sp. nov. (Chilopoda: Geophilomorpha: Ballophilidae) is fully described and illustrated on the basis of specimens collected in Yasuní Scientific Station and Jatun Sacha Biological Station, both located in the Ecuadorian Amazon. The new species is characterized by having the internal edge of the forcipular tarsungulum completely smooth, this trait being shared by six other Neotropical members of the genus Ityphilus Cook, 1899; and another species (I. cifuentesi Cupul Magaña, 2014) from the transition area between the Neotropical and Nearctic regions. Ityphilus grismadoi sp. nov. is distinguished from these seven species by the low number of leg-bearing segments (37, 39), and the very small body size (7–9 mm in length) and for a confident identification it is compared in detail with those having a roughly similar range of leg-bearing segments. This is the first record of the genus Ityphilus from Ecuador and the second report of a ballophilid centipede from the country (the other represented by Zygethmus pantenus Chamberlin, 1957). A key to the Neotropical members of Ityphilus with forcipular tarsungulum smooth (including I. cifuentesi) is also given.

http://zoobank.org/urn:lsid:zoobank.org:pub:32F77890-9DC5-47AC-A794-29C4437C3B93http://zoobank.org/urn:lsid:zoobank.org:act:3EB64970-F159-4C6E-B9FF-AF9D09128553     

Changes in heart ultrastructure during development of Strigamia maritima leach (Myriapoda,Chilopoda, Geophilidae)

The heart ultrastructure of 4 instars of Strigamia maritima (Myriapoda, Chilopoda, Geophilomorpha) (from 2 weeks to 5 years after hatching) is described and compared morphometrically. The single-layered, circular myofibers extend from middorsal to midventral regions, and are interconnected by short, interdigitating intercalated discs. The cardiac sarcomeres show distinct Z-, I-, and A- bands, but myofilaments do not form a well-ordered array. T-tubules originate from any part of the sarcolemma, forming a network of transverse and longitudinal tubules. The transverse tubules ramify in the heart of the foetus instar. The sarcoplasmic reticulum forms a loose sheath at Z-level, and participates in the formation of dyadic and triadic interior couplings. SR-tubules form peripheral couplings on both sides of the myocardium.Volume and length of the myofibers increase constantly during embryonic instars and the first 4 of 5 adult instars, accompanied with an increase in the volume fraction of contractile elements and mitochondria. New sarcomeres are formed abluminally and distally in the fibers, and sarcomeres increase in diameter. Myofibrils become better aligned, longitudinally in the fiber. The growth rate is reduced in the 4th adult instar, and the rough sarcoplasmic reticulum disappears in the 5th instar.     

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, ?? , ??–??.     

On the true identity of Schendylurus (Schendylotyn) integer Chamberlin, 1926, a termitophilous ballophilid centipede (Chilopoda: Geophilomorpha)

Schendylurus (Schendylotyn) integer Chamberlin, 1926, originally described as a member of the Schendylidae, is transferred here to the Ballophilidae as Taeniolinum integer n. comb. and redescribed after the type specimen. Taeniolinum setosum guadeloupensis Demange and Pereira, 1985 is elevated to specific rank.     

Selected body temperatures in the lizard Lacerta vivipara: Variation within and between populations

1. 1.|Selected body temperatures (SBT) of adult male, female and subadult Lacerta vivipara from a Belgian population, were measured monthly in a laboratory thermogradient.

2. 2.|Monthly mean SBTs varied between 29.9 and 34.0°C and differed significantly among months in all three lizard groups, and among lizard groups in 4 out of 6 months.

3. 3.|Evidence for a positive relationship between monthly SBT and air temperature was found in the subadults, but not in the adult lizards.

4. 4.|Monthly mean SBTs measured in this study were consistently higher (mean difference = 2.0°C) than those obtained by Patterson and Davies (1978) in a similar study on Lacerta vivipara from southern England.

The segmentation cascade in the centipede Strigamia maritima: involvement of the Notch pathway and pair-rule gene homologues

The centipede Strigamia maritima forms all of its segments during embryogenesis. Trunk segments form sequentially from an apparently undifferentiated disk of cells at the posterior of the germ band. We have previously described periodic patterns of gene expression in this posterior disc that precede overt differentiation of segments, and suggested that a segmentation oscillator may be operating in the posterior disc. We now show that genes of the Notch signalling pathway, including the ligand Delta, and homologues of the Drosophila pair-rule genes even-skipped and hairy, show periodic expression in the posterior disc, consistent with their involvement in, or regulation by, such an oscillator. These genes are expressed in a pattern of apparently expanding concentric rings around the proctodeum, which become stripes at the base of the germ band where segments are emerging. In this transition zone, these primary stripes define a double segment periodicity: segmental stripes of engrailed expression, which mark the posterior of each segment, arise at two different phases of the primary pattern. Delta and even-skipped are also activated in secondary stripes that intercalate between primary stripes in this region, further defining the single segment repeat. These data, together with observations that Notch mediated signalling is required for segment pattern formation in other arthropods, suggest that the ancestral arthropod segmentation cascade may have involved a segmentation oscillator that utilised Notch signalling.     

Variation in sexual size dimorphism among populations: testing the differential‐plasticity hypothesis

Sexual size dimorphism (SSD) is a common phenomenon in animals and varies widely among species and among populations within species. Much of this variation is likely due to variance in selection on females vs. males. However, environmental variables could have different effects on females vs. males, causing variation in dimorphism. In this study, we test the differential‐plasticity hypothesis, stating that sex‐differential plasticity to environmental variables generates among‐population variation in the degree of sexual dimorphism. We examined the effect of temperature (22, 25, 28, and 31 °C) on sexual dimorphism in four populations of the cockroach Eupolyphaga sinensis Walker (Blattaria: Polyphagidae), collected at various latitudes. We found that females were larger than males at all temperatures and the degree of this dimorphism was largest at the highest temperature (31 °C) and smallest at the lowest temperature (22 °C). There is variation in the degree of SSD among populations (sex*population interaction), but differences between the sexes in their plastic responses (sex*temperature interaction) were not observed for body size. Our results indicated that sex‐differential plasticity to temperature was not the cause of differences among populations in the degree of sexual dimorphism in body size.     

The centipede Strigamia maritima: what it can tell us about the development and evolution of segmentation

One of the most fundamental features of the body plan of arthropods is its segmental design. There is considerable variation in segment number among arthropod groups (about 20-fold); yet, paradoxically, the vast majority of arthropod species have a fixed number of segments, thus providing no variation in this character for natural selection to act upon. However, the 1000-species-strong centipede order Geophilomorpha provides an exception to the general rule of intraspecific invariance in segment number. Members of this group, and especially our favourite animal Strigamia maritima, may thus help us to understand the evolution of segment number in arthropods. Evolution must act by modifying the formation of segments during embryogenesis. So, how this developmental process operates, in a variable-segment-number species, is of considerable interest. Strigamia maritima turns out to be a tractable system both at the ecological level of investigating differences in mean segment number between populations and at the molecular level of studying the expression patterns of developmental genes. Here we report the current state of play in our work on this fascinating animal, including our recent finding of a double-segment periodicity in the expression of two Strigamia segmentation genes, and its possible implications for our understanding of arthropod segmentation mechanisms in general.     

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.     

A study of the diversity and geographical variation in numbers of leg‐bearing segments in centipedes (Chilopoda: Geophilomorpha) in north‐western Europe

Five species of geophilomorphs, Strigamia maritima (Leach, 1817), Geophilus flavus (De Geer, 1778), Geophilus truncorum Bergsøe and Meinert, 1866, Geophilus proximus C. L. Koch, 1847, and Pachymerium ferrugineum (C. L. Koch, 1835), from various sample sites in north‐western Europe were examined for numbers of leg‐bearing segments. Where data was adequate, mean segment numbers were correlated with latitudinal gradients for each species. Solely in S. maritima and some populations of P. ferrugineum did the results show a highly significant geographic pattern towards more leg‐bearing segments in southern populations of both sexes. As concerns G. proximus, we presented for the first time a remarkable geographic shift towards an increased number of pairs of legs in northern populations. Contrary to the conventional geographic pattern, we found that G. flavus and G. truncorum did not exhibit a north–south increase or decrease in segment number. Although there was no general/universal evidence supporting the occurrence of a significant regression slope between mean segment number and latitude/temperature, more information shows that the overall region‐to‐region segment variation was highly significant in both sexes. In S. maritima and P. ferrugineum mean segment number was correlated with the north–south temperature cline. The same was not observed in G. proximus. Parthenogenesis in G. proximus, and a series of ecological characteristics such as habitat preferences, spatial distribution, and fragmented populations could explain the presence or absence of a geographic patterning of segment number variation along a latitudinal cline. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 899–909.     

Intraspecific variation in segment number in Pachymerium ferrugineum (C. L. Koch, 1835) (Chilopoda: Geophilomorpha) in the south Aegean Archipelago (north-east Mediterranean, Greece)

Geophilomorph centipedes have numerous leg-bearing segments, always an odd number. Previous research has shown the significant role of latitudinal clines and temperature on intraspecific variation, supporting the view that species of geophilomorphs from cold and temperate regions tend to have fewer segments than those from warmer regions. Here, data are presented on segment numbers of Pachymerium ferrugineum (C. L. Koch, 1835) from the south Aegean Archipelago. Within the framework of a study of the centipede fauna of the south Aegean Islands, three adjacent geographical areas with discrete geological histories were studied (Crete, Cyclades, and Dodecanese). There is no evidence to indicate that a latitudinal trend is present across these three main geographical regions. Apart from Crete, there is no demonstration of a cline along the longitudinal axis of the Aegean. However, the insular characteristics of the central and south-east Cyclades could possibly support higher modal segment numbers. In addition, examination of males and females of P. ferrugineum confirmed the existence of latitudinal clines in certain cases among the islands of Crete, Cyclades, and Dodecanese.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 533–539.