Decay of velvet worms (Onychophora), and bias in the fossil record of lobopodians

Duncan JE Murdock 1 Sarah E Gabbott 1 Georg Mayer 0 Mark A Purnell 1 0 Animal Evolution and Development, Institute of Biology, University of Leipzig , Talstrae 33, D-04103 Leipzig , Germany 1 Department of Geology, University of Leicester , University Road, Leicester LE1 7RH , UK Murdock et al. - Decay of velvet worms (Onychophora), and in the fossil record of lobopodians Open Access Decay of velvet worms (Onychophora), and bias in the fossil record of lobopodians Background: Fossil lobopodians, including animals proposed to have close affinity to modern onychophorans, are crucial to understanding the evolution of the panarthropod body plan and the phylum-level relationships between the ecdysozoan groups. Unfortunately, the key features of their anatomy are un-mineralized and subject to biases introduced during death, decay and preservation, yet the extent to which these fossils have been affected by the processes of post-mortem decay is entirely untested. Recent experimental work on chordates has highlighted a profound bias caused by decay, resulting in the erroneous interpretation of badly decayed specimens as primitive members of a clade (stemward slippage). The degree to which this bias affects organisms other than chordates is unknown. Results: Here we use experimental decay of velvet worms (Onychophora) to examine the importance of decay bias in fossil lobopodians. Although we find stemward slippage is not significant in the interpretation of non-mineralized lobopodian fossils, the affect of decay is far from unbiased. Quantitative analysis reveals significant changes in body proportions during decay, a spectrum of decay resistance across anatomical features, and correlated decay of topologically associated characters. Conclusions: These results have significant implications for the interpretation of fossil lobopodian remains, demonstrating that features such as body outline and relative proportions are unreliable for taxonomy or phylogenetic reconstruction, unless decay is taken into account. Similarly, the non-independent loss of characters, due to juxtaposition in the body, during decay has the potential to bias phylogenetic analyses of non-biomineralized fossils. Our results are difficult to reconcile with interpretations of highly decay-prone tissues and structures, such as neural tissue, and complex musculature, in recently described Cambrian lobopodians. More broadly, we hypothesize that stemward slippage is unlikely to be a significant factor among the taphonomic biases that have affected organisms where decay-resistant features of the anatomy are rich in phylogenetically informative characters. Conversely, organisms which possess decay-resistant body parts but have informative characters concentrated in decay-prone tissues will be just as liable to bias as those that lack decay-resistant body parts. Further experimental analysis of decay is required to test these hypotheses. Background Fossilization of remains of non-biomineralized tissue is exceptional, but of critical importance. Such exceptionally preserved fossils from the Early Palaeozoic have transformed our understanding of the early evolution of many animal groups, providing constraints on analyses of evolutionary rates, and direct evidence of how the distinctive body plans of extant organisms evolved (e.g. arthropods [1]). Because they preserve body parts that would be expected to completely decompose soon after death, it is tempting to view these fossils as a faithful record of the anatomy of ancient animals and the diversity of faunas, but this is not something that can be assumed. Our view is obscured by the taphonomic filters of decay and fossilization, and it is vital that these filters are understood if we are to obtain a meaningful biological signal from these fossils. Experimental taphonomy aims to tease apart these filters, with much effort focused on recognizing the biases introduced by decay [2,3]. Recent work has highlighted the importance of understanding the sequence of loss of 2014 Murdock et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. anatomical characters [4,5], revealing a pattern of early decay of synapomorphies relative to symplesiomorphies that causes stemward slippage, whereby fossil taxa are placed in more basal positions than they should be due to non-random decay of the phylogenetic signal encoded in their anatomy. The pervasiveness of this bias, and whether some groups of animals are more susceptible than others is an area worth investigating; it may well be a very widespread phenomenon [6] and recent in silico simulated fossilization studies support this view [7]. Fossil lobopodians include animals proposed to have close affinity to modern onychophorans. They have a crucial role in understanding the evolution of the panarthropod body plan and the phylum-level relationships between the ecdysozoan groups [8], yet the extent to which these fossils have been affected by the processes of postmortem decay is entirely untested. Here we investigate this through analysis of decay on onychophorans. The precise relationships between the fossil taxa occupying the onychophoran stem is under much debate [9-11], but modern onychophorans possess a range of characters including some that are unique to extant members of the clade and others that are shared by more inclusive groups. As such they are an appropriate model to investigate decay in both total-group onychophorans and their immediate sister groups. Our study is the first experimental analysis of stemward slippage in invertebrates, investigating character decay in onychophorans and the implications for understanding the fossil record of lobopodians. Results and discussion Within hours of death the onychophoran body flexes, generally a relative lengthening of the ventral side with arching back of the anterior and/or posterior resulting in an S-shaped, U-shaped or entirely curled body shape. (Onychophoran decay is summarized in Table 1 and Figures 1, 2 and 3. Details of the decay trajectory of each character examined are provided in Additional files 3, 4, 5 and 6). Flexing is most pronounced in the first 24 hours and continues to day 3, after which time the curvature of the body does not increase. The first signs of decay are the breakdown of the procuticle and separation of the outer cuticle and the epidermis. Body proportions also change (Figure 2 and Additional file 10): the trunk elongates, typically by 10 30%, and bloating results in an increase in width at the mid-point of (...truncated)