Onychophorology, the study of velvet worms, historical trends, landmarks, and researchers from 1826 to 2020 (a literature review)

Velvet worms, also known as peripatus or onychophorans, are a phylum of evolutionary importance that has survived all mass extinctions since the Cambrian period. They capture prey with an adhesive net that is formed in a fraction of a second. The first naturalist to formally describe them was Lansdown Guilding (1797-1831), a British priest from the Caribbean island of Saint Vincent. His life is as little known as the history of the field he initiated, Onychophorology. This is the first general history of Onychophorology, which has been divided into half-century periods. The beginning, 1826-1879, was characterized by studies from former students of famous naturalists like Cuvier and von Baer. This generation included Milne-Edwards and Blanchard, and studies were done mostly in France, Britain, and Germany. In the 1880-1929 period, research was concentrated on anatomy, behavior, biogeography, and ecology; and it is in this period when Bouvier published his mammoth monograph. The next half-century, 1930-1979, was important for the discovery of Cambrian species; Vachon’s explanation of how ancient distribution defined the existence of two families; DNA and electron microscopy from Brazil; and primitive attempts at systematics using embryology or isolated anatomical characteristics. Finally, the 1980-2020 period, with research centered in Australia, Brazil, Costa Rica, and Germany, is marked by an evolutionary approach: from body and behavior to geographic distribution; the discovery of how they form their adhesive net; the reconstruction of Cambrian onychophoran communities, the first experimental taphonomy; the first country-wide map of conservation status (in Costa Rica); the first model of why they survive in cities; the discovery of new phenomena like food hiding, parental feeding investment, and ontogenetic diet shift; and the birth of a new research branch, onychophoran ethnobiology. While a few names often appear in the literature, most knowledge was produced by a mass of researchers who entered the field only briefly.

Morphological and molecular phylogeny of Epiperipatus (Onychophora: Peripatidae): a combined approach

Onychophora, or velvet worms, are a key group for understanding ecdysozoan evolution. It comprises two families: Peripatopsidae, largely of Austral distribution, and Peripatidae, which is circumtropical. The interrelationships between the members of Peripatidae present many taxonomic issues exacerbated in the radiation of the Neotropical species or Neopatida. To understand the phylogeny of Neopatida, and to test the information of such morphological characters, we gathered novel molecular and morphological datasets focusing on Neotropical specimens. Our data were analysed using a combination of parsimony and maximum likelihood for the individual and combined molecular and morphological datasets. An analysis of morphology alone was inconclusive, supporting the notion that morphological characters used in peripatid taxonomy have little power to resolve phylogenetic relationships among higher taxa in Neopatida. However, the analyses of molecular or combined data show a split of the Neotropical species into two clades, which we use to reassign genera. Epiperipatus, as currently understood, is non-monophyletic, because it includes species of monotypic genera. To avoid paraphyly of Epiperipatus, the following new combinations are proposed: Epiperipatus bouvieri (Fuhrmann, 1913), Epiperipatus hitoyensis (Oliveira et al., 2012a), Epiperipatus solorzanoi (Morera-Brenes & Monge-Nájera, 2010) and Epiperipatus sucuriuensis (Oliveira et al., 2015).

Evolutionary History of Major Chemosensory Gene Families across Panarthropoda

Chemosensory perception is a fundamental biological process of particular relevance in basic and applied arthropod research. However, apart from insects, there is little knowledge of specific molecules involved in this system, which is restricted to a few taxa with uneven phylogenetic sampling across lineages. From an evolutionary perspective, onychophorans (velvet worms) and tardigrades (water bears) are of special interest since they represent the closest living relatives of arthropods, altogether comprising the Panarthropoda. To get insights into the evolutionary origin and diversification of the chemosensory gene repertoire in panarthropods, we sequenced the antenna- and head-specific transcriptomes of the velvet worm Euperipatoides rowelli and analyzed members of all major chemosensory families in representative genomes of onychophorans, tardigrades, and arthropods. Our results suggest that the NPC2 gene family was the only family encoding soluble proteins in the panarthropod ancestor and that onychophorans might have lost many arthropod-like chemoreceptors, including the highly conserved IR25a receptor of protostomes. On the other hand, the eutardigrade genomes lack genes encoding the DEG-ENaC and CD36-sensory neuron membrane proteins, the chemosensory members of which have been retained in arthropods; these losses might be related to lineage-specific adaptive strategies of tardigrades to survive extreme environmental conditions. Although the results of this study need to be further substantiated by an increased taxon sampling, our findings shed light on the diversification of chemosensory gene families in Panarthropoda and contribute to a better understanding of the evolution of animal chemical senses.

A Cambrian fossil from the Chengjiang fauna sharing characters with gilled lobopodians and radiodontans

Background: Lobopodians are worm-like animals with simple legs. Probably representing a grade of organization, rather than an explicit clade, some lobopodians are thought to have given rise to both Euarthropoda and Onychophora (velvet worms). Another subset has been referred to as gilled lobopodians, and are characterized by flap-like appendages along the trunk and large, raptorial forelimbs. These animals probably include the ancestors of another important Cambrian group, the Radiodonta: large predatory or filter-feeding stem-arthropods such as Anomalocaris.Results: Parvibellus atavusgen. et sp. nov.from the Early Cambrian Chengjiang fauna of China is a small fossil preserving a distinct cephalic region bearing a pair of lateral projections and a circular, ventral mouth. The trunk bears eleven pairs of flap-like appendages and a short pair of terminal projections. A circular ventral mouth is also seen in Radiodonta and in some gilled lobopodians. Parvibellus atavus, gilled lobopodians and radiodontans also share the character of flap-like appendages along the trunk. However, the new fossil differs from radiodontans and gilled lobopodians by its small size and the absence of enlarged and/or raptorial frontal appendages. It also differs from gilled lobopodians in lacking ventral lobopod limbs, and from radiodontans in lacking stalked eyes. Conclusions: Parvibellus atavus expresses a unique combination of characters among Cambrian arthropods, and could be part of an early radiation of nektonic stem-Euarthropoda. Lobopodians have emerged as a diverse grade of proto-arthropods ('worms with legs'), walking on the substrate of the early Palaeozoic seas. The new fossil hints at a similarly diverse fauna of nektonic (swimming) stem-group arthropods in the Cambrian, from which gilled lobopodians and radiodontans may have evolved.

History of Onychophorology, 1826-2020

Velvet worms, or onychophorans, include placental species and, as a phylum, have survived all mass extinctions since the Cambrian. They capture prey with an extraordinary adhesive net that appears in an instant. The first naturalist to formally mention them was Lansdown Guilding (1797-1831), a British priest from the Caribbean island of Saint Vincent. His life is as little known as the history of the field he initiated, onychophorology. This is the first general history of onychophorology, and I have divided it into half century periods. The beginning, 1826-1879, was defined by former students of great names in the history of biology, like Cuvier and von Baer. This generation included Milne-Edwars and Blanchard, and the greatest advances came from France, with smaller but still important contributions from England and Germany. In the 1880-1929 period, work concentrated in anatomy, behavior, biogeography and ecology, but of course the most important work was Bouvier’s mammoth monograph. The next half century, 1930-1979, was important for the discovery of Cambrian species; Vachon’s explanation of how ancient distribution defined the existence of two families; Pioneer DNA and electron microscopy from Brazil; and primitive attempts at systematics using embryology or isolated anatomical characteristics. Finally, the 1980-2020 period, with research centered in Australia, Brazil, Costa Rica and Germany, is marked by an evolutionary approach to everything, from body and behavior to distribution; for the solution of the old problem of how they form their adhesive net and how the glue works; the reconstruction of Cambrian onychophoran communities, the first experimental taphonomy; the first country-wide map of conservation status (from Costa Rica); the first model of why they survive in cities; the discovery of new phenomena like food hiding, parental feeding investment and ontogenetic diet shift; and for the birth of a new research branch, Onychophoran Ethnobiology, founded in 2015. While a few names appear often in the literature, most knowledge was produced by a mass of researchers who entered the field only briefly.

Systematics of the Peripatopsis clavigera species complex (Onychophora : Peripatopsidae) reveals cryptic cladogenic patterning, with the description of five new species

During the present study, DNA sequence data, gross morphology and scanning electron microscopy (SEM) were used to examine cryptic species boundaries in the velvet worm, Peripatopsis clavigera species complex, from the southern Cape Afrotemperate forest belt in South Africa. Sequence data were generated for the mitochondrial COI and the nuclear 18S rRNA loci and phylogenetically analysed using both a Bayesian inference and a maximum-likelihood approach. Both the COI data and the combined DNA sequence topology (COI+18S) revealed the presence of five clades within the Peripatopsis clavigera species complex, and revealed that specimens from Tulbagh were distantly related and represented a sixth clade. The evolutionary distinction of the five clades was corroborated to varying degrees by the four species-delimitation methods (ABGD, PTP, GMYC and STACEY); however, both the gross morphological data and the SEM provided limited diagnostic differences between the five clades. Furthermore, the COI haplotype network and phylogeographic analyses provided evidence of genetic isolation between lineages that are currently syntopic. The distribution of genealogically exclusive and widespread maternal lineages was atypical among velvet worms and did not reflect the general trend of genetic and geographical isolation. Instead, lineages exhibited admixture among localities, a result most likely due to fluctuations in climatic conditions affecting the southern Cape Afrotemperate forest during the Pliocene–Pleistocene period as evident from our divergence time estimations. Four novel, narrow-range endemic species – P. ferox, sp. nov., P. mellaria, sp. nov., P. edenensis, sp. nov. and P. mira, sp. nov. – are described within the P. clavigera species complex, whereas the Tulbagh specimens are described as P. tulbaghensis, sp. nov. Collectively, these results demonstrate that Peripatopsis likely contains several undescribed species.

Functional morphology of a lobopod: case study of an onychophoran leg

Segmental, paired locomotory appendages are a characteristic feature of Panarthropoda—a diversified clade of moulting animals that includes onychophorans (velvet worms), tardigrades (water bears) and arthropods. While arthropods acquired a sclerotized exoskeleton and articulated limbs, onychophorans and tardigrades possess a soft body and unjointed limbs called lobopods, which they inherited from Cambrian lobopodians. To date, the origin and ancestral structure of the lobopods and their transformation into the jointed appendages are all poorly understood. We therefore combined high-resolution computed tomography with high-speed camera recordings to characterize the functional anatomy of a trunk lobopod from the onychophoran Euperipatoides rowelli . Three-dimensional reconstruction of the complete set of muscles and muscle fibres as well as non-muscular structures revealed the spatial relationship and relative volumes of the muscular, excretory, circulatory and nervous systems within the leg. Locomotory movements of individual lobopods of E. rowelli proved far more diverse than previously thought and might be governed by a complex interplay of 15 muscles, including one promotor, one remotor, one levator, one retractor, two depressors, two rotators, one flexor and two constrictors as well as muscles for stabilization and haemolymph control. We discuss the implications of our findings for understanding the evolution of locomotion in panarthropods.

The conservation status of Costa Rican velvet worms (Onychophora): geographic pattern, risk assessment and comparison with New Zealand velvet worms

Introduction: Charismatic species, like the panda, play an important role in conservation, and velvet worms arguably are charismatic worms. Thanks to their extraordinary hunting mechanism, they have inspired from a female metal band in Japan, to origami worms in Russia and video game monsters in the USA. Objective: To assess their conservation status in Costa Rica (according to data in the UNA Onychophora Database) and compare it with equivalent data from elsewhere. Methods: we located all collection records of the 29 species in the map of the Costa Rican Conservation Network. Results: We found that seven species are protected inside Forest Reserves, five in Protected Zones, four in Wildlife Refuges, two in National Parks and one, Principapillatus hitoyensis, in a strictly pristine Biological Reserve. The largest species in the world, Peripatus solorzanoi, occurs both inside a Forest Reserve and in protected private land. Protection inside Costa Rican nature areas is enforced year-round by personnel that includes armed guards and is supported by educational programs in surrounding communities. Twelve species have not been found in protected areas, but in Costa Rica, all biological species, named and unnamed, are protected by law and cannot be legally collected, or exported, without technically issued permits. Conclusion: Like in the only other country with similar information (New Zealand), the conservation of onychophorans seems to be of least concern for at least two thirds of the known Costa Rican species. Epiperipatus isthmicola, recently rediscovered after a century of absence in collections, can be considered Threatened because nearly all of its natural habitat has now been covered by a city.