Social behaviour in an Australian velvet worm, Euperipatoides rowelli (Onychophora : Peripatopsidae)

Article · September 2005with914 Reads
DOI: 10.1017/S0952836905007090 · Source: OAI
Abstract
Onychophora lead a cryptic lifestyle as predators in decaying logs and leaf litter. Hence, very little is known about their behaviour. They are generally assumed to possess only a limited behavioural repertoire, even though their surprisingly evolved brain suggests otherwise. Our studies on the Australian species Euperipatoides rowelli show for the first time that onychophorans are indeed capable of complex behaviour. Euperipatoides rowelli individuals form aggregations of up to 15 females, males and young. These aggregations are not random assemblages, but close social groups organized in a hierarchy based on female dominance. Food is hunted collectively, but the dominant female of a group feeds alone, before other females, males and young. Hierarchy within a group is established by aggressive-dominant and passive-subordinate behaviours, the latter leading to tolerance of body contact and aggregation. Euperipatoides rowelli from foreign groups, i.e. from different logs, are met with intense aggression, and individuals rarely aggregate. The reasons for this aggression are not clear, but we suggest that its origins lie in kin recognition. The evolution of social behaviour within the Onychophora is discussed with respect to their ecology, population genetics and phylogeny.
    • The onychophoran jaws are not only used for puncturing the prey ' s cuticle but also for biting rivals—a behavior that occurs frequently in captivity ( Fig . 1G ; Reinhard and Rowell 2005 ) .
    [Show abstract] [Hide abstract] ABSTRACT: Onychophorans are carnivorous, terrestrial invertebrates that occur in tropical and temperate forests of the Southern Hemisphere and around the Equator. Together with tardigrades, onychophorans are regarded as one of the closest relatives of arthropods. One of the most peculiar features of onychophorans is their hunting and feeding behavior. These animals secrete a sticky slime, which is ejected via a pair of slime-papillae, to entangle the prey. After the prey has been immobilized, its cuticle is punctured using a pair of jaws located within the mouth. These jaws constitute internalized appendages of the second body segment and are innervated by the deutocerebrum; thus, they are homologous to the chelicerae of chelicerates, and to the (first) antennae of myriapods, crustaceans, and insects. The jaws are also serial homologs of the paired claws associated with each walking limb of the trunk. The structure of the jaws is similar in representatives of the two major onychophoran subgroups, the Peripatidae and Peripatopsidae. Each jaw is characterized by an outer and an inner blade; while the outer blade consists only of a large principal tooth and up to three accessory teeth, the inner blade bears numerous additional denticles. These denticles are separated from the remaining part of the inner jaw by a diastema and a soft membrane only in peripatids. The onychophoran jaws are associated with large apodemes and specialized muscles that enable their movement. In contrast to the mandibles of arthropods, the onychophoran jaws are moved along, rather than perpendicular to, the main axis of the body. Our elemental analysis reveals an increased incorporation of calcium at the tip of each blade, which might provide rigidity, whereas there is no evidence for incorporation of metal or prominent mineralization. Stability of the jaw might be further facilitated by the cone-in-cone organization of its cuticle, as each blade consists of several stacked, cuticular elements. In this work, we summarize current knowledge on the jaws of onychophorans, which are a characteristic feature of these animals. © The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: journals.permissions@oup.com.
    Full-text · Article · Mar 2015
    • This species occurs at high densities allowing large sample sizes across relatively narrow contact zones (Barclay, Ash & Rowell, 2000a), is known to be strongly spatially genetically structured at Tallaganda based on microsatellite data (Sunnucks & Wilson, 1999), and morphologically aberrant individuals occasionally occur where certain catchments meet (Sunnucks & Tait, 2001), indicating that hybridization probably occurs between the catchment-specific, genetically and morphologically distinguishable groups (races herein). Furthermore, this species has a well-characterized natural history (Curach & Sunnucks, 1999; Sunnucks et al., 2000; Barclay et al., 2000a; Barclay, Rowell & Ash, 2000b; Sunnucks & Tait, 2001; Reinhard & Rowell, 2005), which aids in the interpretation of results. Here, we used genetic markers and phenotypes to characterize a previously unstudied contact zone between two of these races to determine whether hybridization occurs, and whether two potential explanations for genetic structuring – assortative mating (Dobzhansky, 1940) and reduced hybrid survival, a potential component of hybrid breakdown (Alatalo et al., 1990) – are applicable to this contact zone.
    [Show abstract] [Hide abstract] ABSTRACT: Genetic studies have revealed a large degree of previously unappreciated diversity in morphologically conserved taxa. To understand the implications of this phenomenon, studies investigating the processes responsible for generating and maintaining functional and neutral diversity within such taxa are needed. With this aim, patterns of differentiation across a contact zone between two catchment-specific, genetically- and subtly-morphologically-distinguishable races of the onychophoran Euperipatoides rowelli Reid 1996 at the Tallaganda State Forest study system, Australia were quantified using diagnostic body-pattern differences, microsatellite markers, and the cytochrome c oxidase 1 (COI) mitochondrial gene. These data were used to test if hybridization occurred and if reduced survival of hybrids compared to non-hybrids and / or assortative mating were potentially important factors in retaining the divergence between these races, which probably arose during isolation in Pleistocene glacial refuges. It was found that hybrids at the focal contact zone do not have reduced embryo-to-adult survival compared to non-hybrids, and that races apparently freely interbreed without substantial assortative mating, consistent with little or no cost to hybridization. Nonetheless, at their respective transect-ends, the races remain distinct. This phenomenon was attributed to the elevated location of the contact zone, which likely makes it poor habitat for E. rowelli, and thus may restrict dispersal and gene flow. There was also tentative evidence for a relaxed selection against hybridization in the hybrid zone and the relative importance of these two explanations will require separate investigation.
    Article · Jan 2014
    • Onychophoran biology renders them extremely susceptible to desiccation outside logs [26,27], so dispersal is risky. Even without postzygotic isolation, reproductive success after dispersal is likely to be lowered by features of the mating system and complex social biology including high aggression of females towards males from 'foreign' logs [23,25,28]. Gene flow between microgeographic regions should be low because the cooler, drier ridges between catchments are lower quality habitat housing fewer E. rowelli [26,85,86].
    [Show abstract] [Hide abstract] ABSTRACT: Phylogeographic studies provide a framework for understanding the importance of intrinsic versus extrinsic factors in shaping patterns of biodiversity through identifying past and present microevolutionary processes that contributed to lineage divergence. Here we investigate population structure and diversity of the Onychophoran (velvet worm) Euperipatoides rowelli in southeastern Australian montane forests that were not subject to Pleistocene glaciations, and thus likely retained more forest cover than systems under glaciation. Over a ~100 km transect of structurally-connected forest, we found marked nuclear and mitochondrial (mt) DNA genetic structuring, with spatially-localised groups. Patterns from mtDNA and nuclear data broadly corresponded with previously defined geographic regions, consistent with repeated isolation in refuges during Pleistocene climatic cycling. Nevertheless, some E. rowelli genetic contact zones were displaced relative to hypothesized influential landscape structures, implying more recent processes overlying impacts of past environmental history. Major impacts at different timescales were seen in the phylogenetic relationships among mtDNA sequences, which matched geographic relationships and nuclear data only at recent timescales, indicating historical gene flow and/or incomplete lineage sorting. Five major E. rowelli phylogeographic groups were identified, showing substantial but incomplete reproductive isolation despite continuous habitat. Regional distinctiveness, in the face of lineages abutting within forest habitat, could indicate pre- and/or postzygotic gene flow limitation. A potentially functional phenotypic character, colour pattern variation, reflected the geographic patterns in the molecular data. Spatial-genetic patterns broadly match those in previously-studied, co-occurring low-mobility organisms, despite a variety of life histories. We suggest that for E. rowelli, the complex topography and history of the region has led to interplay among limited dispersal ability, historical responses to environmental change, local adaptation, and some resistance to free admixture at geographic secondary contact, leading to strong genetic structuring at fine spatial scale.
    Full-text · Article · Dec 2013
    • Three types of pairs were established, with the following relationships between individuals: coming from pairs of regions with areas of geographic contact, coming from pairs of regions with no areas of geographic contact, or, as a control, coming from the same region (Table 2A). Pairs were checked weekly for 12 week and it was noted if the individuals were closely aggregated, a behaviour that has been shown to require cooperation from both individuals and to occur at rates inversely proportionate to those of aggressive behaviours between individuals (Reinhard & Rowell 2005). The portion of occasions on which pairs were closely aggregated was compared across pair types (adjacent regions, non-adjacent regions, same regions) using a single factor ANOVA (Quinn & Keough 2002).
    [Show abstract] [Hide abstract] ABSTRACT: Genetic studies have revealed a large degree of previous unappreciated diversity in morphologically conserved taxa. As most of these studies have used neutral genetic markers, it is unclear if the revealed groups are functionally different. To understand this, studies investigating the processes responsible for generating and maintaining functional and neutral diversity are needed. With this aim, life-history differences between two catchment-specific forms of the onychophoran Euperipatoides rowelli at Tallaganda State Forest, New South Wales, were quantified and the contact zone between these two forms was characterized using diagnostic body-pattern differences, microsatellite markers, and the cytochrome c oxidase 1 (COI) mitochondrial gene. These data were used to test for the following: extent of life history differentiation, presence of selection on body pattern and COI, reduced fitness of hybrids compared to non-hybrids, and presence of assortative mating between forms. Forms were found to differ in body mass in the wild and growth rate in a common environment, but not in birth schedule. On the basis of environmental and genetic data, differences in body size in the wild were attributed largely to phenotypic plasticity, but differences in growth rate apparently had a large genetic component. The hybrid zone characterization revealed that forms apparently freely interbreed without substantial assortative mating, consistent with little or no cost to hybridization. Nonetheless, at their respective ends of the transect, the forms remain distinct. This phenomenon was attributed to the elevated location of the contact zone, which likely makes it poor habitat for E. rowelli, and thus a substantial barrier to dispersal and gene flow. However, a scenario of stronger selection against hybridization outside the hybrid zone than inside the hybrid zone could not be rejected. Region diagnostic COI haplotypes had different nucleotide sequences, but no evidence was found for selection underlying the spatial pattern of these haplotypes, consistent with them encoding the same amino acid sequence and thus being functional equivalent. Evidence for divergent selection on body colour pattern was detected, but the importance of this finding is unclear due to methodological concerns. Comparison with a previously characterized E. rowelli hybrid zone at Tallaganda indicated multiple factors are responsible for the distinctiveness of the catchment-specific forms of E. rowelli, and that differences in life history traits among interacting populations or species may not result in low fitness hybrids. Further, this comparison showed environmental features may be as important as organismal features in determining patterns of functional and neutral diversity.
    Full-text · Thesis · Apr 2010 · Australian Journal of Zoology
    • Saproxylic organisms, such as P. australis, are prone to the formation of small, isolated populations due primarily to the fragmented distribution of forested habitats in eastern Australia and the scattered distribution of rotting logs within these forests (e.g. Barclay et al. 2000a; Reinhard and Rowell 2005). The imposition that this population structure may have on population mixing in P. australis is further exacerbated by the species' secondary flightlessness (Roth 1977), which limits its dispersal abilities, resulting in restricted gene flow between populations, and hence substantial genetic differentiation among populations (MacEachern 2001).
    [Show abstract] [Hide abstract] ABSTRACT: An ability to recognise and discriminate between group and non-group members is essential for most group-living species. Several different sensory modalities may be utilised for social recognition, the most notable of which is olfaction. Among insects, members of the order Blattodea (cockroaches, termites) exhibit a diverse range of social systems and provide an excellent model for examining the role of chemical communication in group discrimination. We experimentally tested the importance of chemical cues in the association preferences of the subsocial Australian wood-boring cockroach, Panesthia australis. Using a series of dichotomous choice trials, we found that individuals preferred conspecific odour cues over those of an unscented peatmoss control. We then gave cockroaches a choice between the odour cues of cockroaches from different logs, and found that they did not exhibit a preference for the cues of individuals from their own log versus those from different logs within the same locality. However, cockroaches exhibited a strong preference for cues taken from individuals from a geographically distant population. Our findings suggest that P. australis engages in group discrimination, and that patterns of association may reflect an underlying preference for unfamiliar and/or genetically dissimilar individuals in a species encumbered by restricted gene flow.
    Full-text · Article · Jan 2009
  • [Show abstract] [Hide abstract] ABSTRACT: PET cerebral blood flow (CBF) methods require tissue and arterial blood radioactivity measurements to yield absolute values. The authors have developed a method to estimate CBF without a measured input function. For N pixels and M scan frames, the authors estimate N+M parameters (N flow values and M input function integrals) from N×M measurements with weighted least squares using the iterative Gauss-Newton (GN) algorithm. Tracer distribution volume is assumed to be known. This method was tested with simulated and human image data. Simulation GN errors in whole brain CBF were -3±2%, with uniform percent errors for all flow values. GN image quality was comparable to that obtained from algorithms which require the measured input function. Results with actual scan data (8 subjects, 4 studies each) had errors in global flow of -77±3% due to violations of the model assumptions, particularly tissue heterogeneity. Use of a modified algorithm which included inter-pixel variations in the distribution volume to account for heterogeneity reduced the bias but the results are overly sensitive to the assumed value of distribution volume variability. Although this method can theoretically provide absolute CBF, it will be useful in practice only if its large sensitivity to model inaccuracies can be controlled
    Conference Paper · Jan 1994 · Australian Journal of Zoology
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April 2000 · Journal of Zoology · Impact Factor: 1.88
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