Comparative studies on the structure and development of the venom‐delivery system of centipedes,and a hypothesis on the origin of this evolutionary novelty

The venom‐injecting forcipules of centipedes represent an evolutionary novelty that appeared in the centipede stem lineage more than 400 Ma. No other lineage of arthropods (or indeed of animals) has evolved claws for injecting venom from a pair of walking legs. However, little is known of the development, ultrastructure, or detailed function of centipede forcipules. Here, we provide comparative structural information on the venom duct apparatus that is the main functional system within each forcipule, based on scanning electron microscopy and transmission electron microscopy studies. We also give comparative developmental information, using DAPI staining, on embryonic forcipules from the four main centipede orders, including Scutigeromorpha. The photographs of Scutigera embryos we present are the first to be published for any species belonging to this order. The structure of the venom apparatus within each forcipule represents a discrete element of the novelty, whose origin requires a special explanation. This is in contrast to the novel external shape of the forcipules, which can be arrived at gradually by a series of changes from the starting point of a standard walking leg. Drawing on a proposed structural homology between venom glands and epidermal glands, we present a hypothesis of how the venom gland and duct may have arisen in evolution.     

Detecting taxonomic signal in an under-utilised character system: geometric morphometrics of the forcipular coxae of Scutigeromorpha (Chilopoda)

To date, the forcipules have played almost no role in determining the systematics of scutigeromorph centipedes though in his 1974 review of taxonomic characters Markus Würmli suggested some potentially informative variation might be found in these structures. Geometric morphometric analyses were used to evaluate Würmli's suggestion, specifically to determine whether the shape of the forcipular coxa contains information useful for diagnosing species. The geometry of the coxae of eight species from the genera Sphendononema, Scutigera, Dendrothereua, Thereuonema, Thereuopoda, Thereuopodina, Allothereua and Parascutigera was characterised using a combination of landmark- and semi-landmark-based sampling methods to summarize group-specific morphological variation. Canonical variates analysis of shape data characterizing the forcipular coxae indicates that these structures differ significantly between taxa at various systematic levels. Models calculated for the canonical variates space facilitate identification of the main shape differences between genera, including overall length/width, curvature of the external coxal margin, and the extent to which the coxofemoral condyle projects laterally. Jackknifed discriminant function analysis demonstrates that forcipular coxal training-set specimens were assigned to correct species in 61% of cases on average, the most accurate assignments being those of Parascutigera (Parascutigera guttata) and Thereuonema (Thereuonema microstoma). The geographically widespread species Thereuopoda longicornis, Sphendononema guildingii, Scutigera coleoptrata, and Dendrothereua linceci exhibit the least diagnostic coxae in our dataset. Thereuopoda longicornis populations sampled from different parts of East and Southeast Asia were significantly discriminated from each other, suggesting that, in this case, extensive synonymy may be obscuring diagnosable inter-species coxal shape differences.     

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.     

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.     

Geographic patterning of variation in segment number in geophilomorph centipedes: clines and speciation

SUMMARY Since their origin as a metameric group, arthropods have diversified considerably in their number of segments. Present-day geophilomorph centipedes provide a model system for investigating the evolutionary origins of this diversification, because they exhibit intraspecific variation in segment number. (This variation is, however, derived; it is not a plesiomorphic condition within the Chilopoda.) Previous studies have shown that there are significant differences in segment number between populations within several geophilomorph species. In one (arguably two) species, it has been demonstrated that there is a particular form of geographic patterning of the variation, namely a latitudinal cline, with the segment number decreasing with increasing distance north. Here, we provide additional data on four more species, all of which show evidence of a latitudinal cline in either one or both sexes. It is therefore becoming clear that this is a general phenomenon, applying widely (perhaps universally) across the Geophilomorpha, a group consisting of some 1000 known species. It may be that latitudinal clines are a frequent part of the speciation cycle in this group.     

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.     

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 .     

Responses of juvenile terrestrial salamanders to introduced (Lithobius forficatus) and native centipedes (Scolopocryptops sexspinosus)

When introduced species invade ecosystems, alterations in community structure can emerge from the competitive and predatory interactions that occur between introduced and native guild members. Because a number of recent studies have shown that large predatory invertebrates can both compete with and prey on small vertebrates and because introductions of non-native species may play a role in amphibian declines, the effects of introduced centipedes Lithobius forficatus and native centipedes Scolopocryptops sexspinosus on juveniles of the red-backed salamander Plethodon cinereus were examined. In laboratory arenas, juvenile salamanders exhibited submissive behaviour in response to the odours of both species of centipede. There were no significant differences in salamander response to the two centipede odour treatments, but compared to controls, juveniles of P. cinereus spent significantly more time in escape and in a flattened submissive posture when presented with native centipede odours. Despite significant size differences between centipedes and juvenile salamanders, no predation of salamanders by either species of centipede occurred in any pairings. Juveniles exhibited more chemosensory behaviour towards native centipedes and towards their odours and exhibited marked reductions in aggressive posturing when centipedes were present. Field and laboratory data suggest that juveniles of P. cinereus and centipedes were negatively associated. In laboratory trials, the native centipede excluded juvenile salamanders from cover objects and we found fewer instances of co-occurrence in the field than expected. These studies are the first to examine the behavioural interactions between juveniles of P. cinereus and invertebrate predators, one introduced and one native, of eastern deciduous forest-floor food webs.     

The arts and human nature: evolutionary aesthetics and the evolutionary status of art behaviours

This essay reviews one of the most recent books in a trend of new publications proffering evolutionary theorising about aesthetics and the arts—themes within an increasing literature on aspects of human life and human nature in terms of evolutionary theory. Stephen Davies’ The Artful Species links some of our aesthetic sensibilities with our evolved human nature and critically surveys the interdisciplinary debate regarding the evolutionary status of the arts. Davies’ engaging and accessible writing succeeds in demonstrating the maturity and scope of the field and his critique is timely and unparalleled. A laudable effort, however it may have benefited from espousing a co-evolutionary model more explicitly. Moreover there may be reason to question the usefulness of the standard set of distinctions (‘adaptation’, ‘spandrel’, ‘technology’) that Davies appeals to.     

Behavioral interactions between salamanders and centipedes: competition in divergent taxa

Red-backed salamanders, Plethodon cinereus, use territorialadvertisement in the form of agonistic displays and pheromonalscent marking as a mechanism for intraspecific interferencecompetition. Although ecological and behavioral interactionsamong species of salamanders have been well studied, littleis known about the interactions between territorial P. cinereusand other ecologically similar species, such as large predatoryinvertebrates. Our field data indicate that P. cinereus anda large syntopic centipede, Scolopocryptops sexspinosus, exhibitnegative spatial associations in natural habitats, possiblyindicating interspecific territoriality. Only seven instancesof salamander/centipede co-occurrence were recorded from a fieldsample of 247 occupied cover objects. Cover object size waspositively correlated with salamander SVL (tip of the snoutto the anterior end of the cloaca), but there was no correlationof cover object size to centipede length. Data on the abilityof P. cinereus to differentiate among chemicals on the substratesuggest that visual cues are not necessary to elicit a territorialresponse from intruding salamanders. Although in laboratorytrials salamanders behaved similarly toward intruders of bothspecies, biting was directed only toward centipedes. Salamandersspent significantly more time approaching centipedes than theydid approaching other salamanders. Approach behavior was oftenassociated with nose tapping and may be an investigative, ratherthan aggressive, behavior. We suggest that territorial P. cinereusrespond similarly to intruding salamanders and centipedes, butthat they escalate more readily to biting centipedes becauseS. sexspinosus is sightless and thus unable to respond to visualsignals.     

Conflict between datasets and phylogeny of centipedes: an analysis based on seven genes and morphology

Although the phylogeny of centipedes has found ample agreement based on morphology, recent analyses incorporating molecular data show major conflict at resolving the deepest nodes in the centipede tree. While some genes support the classical (morphological) hypothesis, others suggest an alternative tree in which the relictual order Craterostigmomorpha, restricted to Tasmania and New Zealand, is resolved as the sister group to all other centipedes. We combined all available data including seven genes (totalling more than 8 kb of genetic information) and 153 morphological characters for 24 centipedes, and conducted a sensitivity analysis to evaluate where the conflict resides. Our data showed that the classical hypothesis is obtained primarily when nuclear ribosomal genes exert dominance in the character data matrix (at high gap costs), while the alternative tree is obtained when protein-encoding genes account for most of the cladogram length (at low gap costs). In this particular case, the addition of genetic data does not produce a more stable hypothesis for deep centipede relationships than when analysing certain genes independently, but the overall conflict in the data can be clearly detected via a sensitivity analysis, and support and stability of shallow nodes increase as data are added.     

SLOWER TEMPO OF MICROEVOLUTION IN ISLAND BIRDS: IMPLICATIONS FOR CONSERVATION BIOLOGY

Whether microevolution on small islands differs from that on larger landmasses is a key question in biology with substantial implications for species conservation. However, due to the difficulties faced in producing adequately replicated samples and in controlling for confounding variables, prior attempts to examine evolutionary questions relating to habitat area and population size have produced equivocal results. Here we show, using experimental design criteria that reduce the potential for such confounding, that bird species on larger landmasses have higher rates of molecular evolution. The study involves a global dataset of 48 independent contrasts for the cytochrome b gene encompassing all possible paired sister species comparisons (from seven orders and 17 families) that were available at the time of dataset assembly. A more rapid evolutionary tempo in larger areas has important ramifications for biodiversity conservation because it indicates a new imperative, beyond that of simply maintaining preexisting genetic diversity, for securing large areas for threatened species. This result suggests that the trend of confining species to limited refugia is likely to be slowing the tempo of microevolution. That effect might constrain the potential for adaptive shifts in response to changing environments such as those associated with global warming.     

Ballooning dispersal using silk: world fauna, phylogenies, genetics and models

Aerial dispersal using silk ('ballooning') has evolved in spiders (Araneae), spider mites (Acari) and in the larvae of moths (Lepidoptera). Since the 17th century, over 500 observations of ballooning behaviours have been published, yet there is an absence of any evolutionary synthesis of these data. In this paper the literature is reviewed, extensively documenting the known world fauna that balloon and the principal behaviours involved. This knowledge is then incorporated into the current evolutionary phylogenies to examine how ballooning might have arisen. Whilst it is possible that ballooning co-evolved with silk and emerged as early as the Devonian (410-355 mya), it is arguably more likely that ballooning evolved in parallel with deciduous trees, herbaceous annuals and grasses in the Cretaceous (135-65 mya). During this period, temporal (e.g. bud burst, chlorophyll thresholds) and spatial (e.g. herbivory, trampling) heterogeneities in habitat structuring predominated and intensified into the Cenozoic (65 mya to the present). It is hypothesized that from the ancestral launch mechanism known as 'suspended ballooning', widely used by individuals in plant canopies, 'tip-toe' and 'rearing' take-off behaviours were strongly selected for as habitats changed. It is contended that ballooning behaviour in all three orders can be described as a mixed Evolutionary Stable Strategy. This comprises individual bet-hedging due to habitat unpredictability, giving an underlying randomness to individual ballooning, with adjustments to the individual ballooning probability being conferred by more predictable habitat changes or colonization strategies. Finally, current methods used to study ballooning, including modelling and genetic research, are illustrated and an indication of future prospects given.     

Intraspecific Variation in Developmental Characters: The Origin of Evolutionary Novelties

Evolutionary developmental biology is inevitably a comparativesubject. However, the taxonomic level at which comparisons canbe made varies widely, and this greatly affects the kind ofinformation that can be gained from the comparison. Broadlyspeaking, high-level comparisons (e.g., between phyla) are moreinformative about phylogenetic pattern and homology, while low-levelcomparisons (e.g., between congeneric species) are more informativeabout evolutionary mechanisms, including speciation. However,so far evolutionary developmental biology has had a relativelyminor input into the traditional territory of population genetics,namely comparisons within species—both within and betweengeographic populations. Yet this area is crucial, as all evolutionarynovelties ultimately arise from intraspecific variation. Here,I address this issue, focusing on the question of how earlyin development novelties arise. To shed light on this question,I discuss two examples of developmental polymorphism withinspecies involving two of the main body axes: anteroposteriorsegmentation in centipedes and left–right asymmetry (chirality)in gastropods.     

On the function of the ultimate legs of some Scolopendridae (Chilopoda,Scolopendromorpha)

The function of the variously shaped ultimate legs of Scolopendridae is briefly reviewed. Their function in Scolopendra heros Girard, 1853, Scolopendra subspinipes Leach, 1815, Scolopendra morsitans (Linnaeus, 1758), Scolopendra galapagoensis Bollman, 1889, Scolopendra hainanum Kronmüller, 2012, Scolopendra spinosissima Kraepelin, 1903 Cormocephalus aurantiipes (Newport, 1844) and Ethmostigmus trigonopodus (Leach, 1817), in which they are least specialised has been investigated. Specimens were tapped with forceps on different parts of the trunk to simulate the attack of a predator. When tapped on the first third of the trunk (near the head), the centipedes attacked the forceps with their forcipules. When tapped on the last third or the ultimate legs, they adopted a warning position, raising the ultimate legs to display the ventral and medial prefemoral spines as well as the spined coxopleural processes. In some cases the centipedes attacked the forceps with the claws of the ultimate legs by chopping down on them after lifting the legs high into the warning position. When tapped in the mid part of the trunk, the centipedes curled sideways to reach the forceps with their forcipules and ultimate legs simultaneously. Scolopendra galapagoensis not only lifted the ultimate legs into the warning position but also the last 3-4 pairs of locomotory legs, presenting their distodorsal prefemoral spines. This resembles the warning posture of some spiders. In addition to their function in warning behaviour, defensive stabbing, ritualised meeting reactions and during courtship behaviour, the ultimate legs may in addition act as hooks and perhaps be involved in species recognition. No evidence was found that the ultimate legs are used to catch prey, nor of prey or predators being held between the prefemora.     

Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys

New World monkeys (NWM) display substantial variation (two orders of magnitude) in body size. Despite this, variation in skull size and associated shape show a conserved allometric relationship, both within and between genera. Maximum likelihood estimates of quantitative ancestral states were used to compare the direction of morphological differentiation with the phenotypic (p(max)) and genetic (g(max)) lines of least evolutionary resistance (LLER). Diversification in NWM skulls occurred principally along the LLER defined by size variation. We also obtained measures of morphological amount and pace of change using our skull data together with published genetic distances to test whether the LLER influenced the amount and pace of diversification. Moreover, data on an ecological factor (diet) was obtained from the literature and used to test the association of this niche-related measure with the morphological diversification. Two strategies were used to test the association of LLER with the morphological and dietary amount and pace of change, one focusing on both contemporary genera and maximum likelihood reconstructed ancestors and the other using only the 16 contemporary genera in a phylogenetic comparative analysis. Our results suggest that the LLER influenced the path, amount, and pace of morphological change. Evolution also occurred away from the LLER in some taxa but this occurred at a slower pace and resulted in a relatively low amount of morphological change. We found that longer branch lengths (time) are associated with larger differences in p(max) orientation. However, on a macroevolutionary scale there is no such trend. Diet is consistently associated with both absolute size differences and morphological integration patterns, and we suggest that this ecological factor might be driving adaptive radiation in NWM. Invasion of diet-based adaptive zones involves changes in absolute size, due to metabolic and foraging constraints, resulting in simple allometric skull diversification along the LLER. While it is clear that evolutionary change occurred along the LLER, it is not clear whether this macroevolutionary pattern results from a conservation of within-population genetic covariance patterns or long-term adaptation along a size dimension or whether both constraints and selection were inextricably involved.     

The mode of sperm transfer in the scolopendromorph centipede:Cormocephalus anceps anceps Porat

The laboratory conditions under which the centipedes were kept and their general behaviour are described. No indication of sexual recognition between adult centipedes was found during studies made of encounters between members of the same or opposite sexes. All displayed the same avoiding reaction on the first encounter and later adopted the defence posture by which fatal attacks were prevented. Where attacks were not successfully countered, biting may or may not be accompanied by injection of poison into the wound. These centipedes are not immune to the poison of their own species, therefore, fatalities and cannibalism can result from aggressive encounters.
The mating behaviour of Cormocephalus anceps was witnessed once in early autumn in South Africa. It was preceded by the typical avoiding reaction and defence posture assumed by either sex towards the other, the male being the more dominant. After adopting this posture, a situation which may last a variable length of time, the subsequent stages of mating behaviour were initiated by the male. The courting behaviour could be followed in five sequences which are described in some detail.
The problems of sperm transfer faced by the Arthropoda evolving towards a wholly terrestrial existence and the many modes adopted by this group are considered together with the recent knowledge of the modes of sperm transfer employed by the four orders of Chilopoda.     

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.