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.

Experimental taphonomy of organelles and the fossil record of early eukaryote evolution

The timing of origin of eukaryotes and the sequence of eukaryogenesis are poorly constrained because their fossil record is difficult to interpret. Claims of fossilized organelles have been discounted on the unsubstantiated perception that they decay too quickly for fossilization. We experimentally characterized the pattern and time scale of decay of nuclei, chloroplasts, and pyrenoids in red and green algae, demonstrating that they persist for many weeks postmortem as physical substrates available for preservation, a time scale consistent with known mechanisms of fossilization. Chloroplasts exhibit greater decay resistance than nuclei; pyrenoids are unlikely to be preserved, but their presence could be inferred from spaces within fossil chloroplasts. Our results are compatible with differential organelle preservation in seed plants. Claims of fossilized organelles in Proterozoic fossils can no longer be dismissed on grounds of plausibility, prompting reinterpretation of the early eukaryotic fossil record and the prospect of a fossil record of eukaryogenesis.

Nucleus preservation in early Ediacaran Weng'an embryo-like fossils, experimental taphonomy of nuclei and implications for reading the eukaryote fossil record

The challenge of identifying fossilized organelles has long hampered attempts to interpret the fossil record of early eukaryote evolution. We explore this challenge through experimental taphonomy of nuclei in a living eukaryote and microscale physical and chemical characterization of putative nuclei in embryo-like fossils from the early Ediacaran Weng'an Biota. The fossil nuclei exhibit diverse preservational modes that differ in shape, presence or absence of an inner body and the chemistry of the associated mineralization. The nuclei are not directly fossilized; rather, they manifest as external moulds. Experimental taphonomy of epidermal cells from the common onion ( Allium cepa ) demonstrates that nuclei are more decay resistant than their host cells, generally maintaining their physical dimensions for weeks to months post-mortem, though under some experimental conditions they exhibit shrinkage and/or become shrouded in microbial biofilms. The fossil and experimental evidence may be rationalized in a single taphonomic pathway of selective mineralization of the cell cytoplasm, preserving an external mould of the nucleus that is itself resistant to both decay and mineral replication. Combined, our results provide both a secure identification of the Weng'an nuclei as well as the potential of a fossil record of organelles that might help arbitrate in long-standing debates over the relative and absolute timing of the evolutionary assembly of eukaryote-grade cells.

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.