Fossils from South China redefine the ancestral euarthropod body plan

Abstract

Background: Early Cambrian Lagerstätten from China have greatly enriched our perspective on the early evolution of animals, particularly arthropods. However, recent studies have shown that many of these early fossil arthropods were more derived than previously thought, casting uncertainty on the ancestral euarthropod body plan. In addition, evidence from fossilized neural tissues conflicts with external morphology, in particular regarding the homology of the frontalmost appendage. Results: Here we redescribe the multisegmented megacheirans Fortiforceps and Jianfengia and describe Sklerolibyon maomima gen. et sp. nov., which we place in Jianfengiidae, fam. nov. (in Megacheira, emended). We find that jianfengiids show high morphological diversity among megacheirans, both in trunk ornamentation and head anatomy, which encompasses from 2 to 4 post-frontal appendage pairs. These taxa are also characterized by elongate podomeres likely forming seven-segmented endopods, which were misinterpreted in their original descriptions. Plesiomorphic traits also clarify their connection with more ancestral taxa. The structure and position of the "great appendages" relative to likely sensory antero-medial protrusions, as well as the presence of optic peduncles and sclerites, point to an overall homology with the anterior head of radiodontans. This is confirmed by our Bayesian phylogeny, which places jianfengiids as the basalmost euarthropods, paraphyletic with other megacheirans, and in contiguity with isoxyids and radiodontans. Conclusions: Sklerolibyon and other jianfengiids expand the disparity of megacheirans and suggest that the common euarthropod ancestor possessed a remarkable phenotypic variability associated with the externalized cephalon, as well as endopods that were already heptopodomerous, which differs from previous hypotheses and observations. These animals also demonstrate that the frontalmost pair of arthrodized appendage is homologous between radiodontans and megacheirans, refuting the claim that the radiodontan frontal appendages evolved into the euarthropod labrum, and questioning its protocerebral identity. This evidence based on external anatomy now constitutes a solid benchmark upon which we should address issues of homology, with the help of carefully examined palaeoneurological data.

A new euarthropod with ‘great appendage’-like frontal head limbs from the Chengjiang Lagerstätte, Southwest China

“…The convergence hypothesis agrees with the interpretation of Budd (2002), who considered the 'great appendage' to represent a pre-antennular appendage that was transformed into the labrum (see Scholtz and Edgecombe, 2006;Cong et al, 2014;Ortega-Hernández et al, 2017;Daley et al, 2018;Park et al, 2018) in the group including euarthropods (see also Eriksson et al, 2003) for which there are lines of evidence pro (e.g., Siewing, 1969;Lauterbach, 1973;Rempel, 1975), et contra (e.g., Walossek and Müller, 1998;Wolff, 2004;Mayer et al, 2014;Aria, 2020). If we subscribe to the hypothesis that the 'great appendage' was lost or reduced into the labrum, then the presence of 'great appendage'-like frontal head limbs require convergence.…”

“…However, the results of two important phylogenies (Daley et al, 2009, Kühl et al, 2009 supporting this theory were criticised by Haug et al (2012b) due to apparent discrepancies in the coding of some characters and taxa. The debate on the nature of radiodonts is not closed yet: the phylogenetic analyses of Vannier, (2013), Vin-ther et al (2014), Yang et al (2015Yang et al ( , 2018, Moysiuk and Caron (2019) and Aria et al (2020) support a 'stem-group' affinity for radiodonts. In this scheme, Bushizheia yangi gen. et sp.…”

The origin and evolution of the euarthropod labrum

“…Although such a homology has sometimes been disputed (e.g. Richter et al 2013;Stein 2010;Aria et al 2020), and of course may be false, it still seems by far the most parsimonious explanation of the data to hand, which converge on the same conclusion from a variety of sources (see discussion in e.g. Ortega-Hernández et al 2017 and.…”

“…This point (which logically follows from the premises) is, however, often disputed, either implicitly or explicitly. For example, Ortega-Hernández (2015) names a scion (Craske and Jefferies 1986;Budd 2001b) of the euarthropods the "Deuteropoda" because of its putative possession of a differentiated deutocerebral appendage that encompasses the entire known upper stem group (and the crown group) of the euarthropods; Liu et al (2016) claim that the appendage of Leanchoilia is likely to be deutocerebral because Leanchoilia is a euarthropod; and similarly, Aria et al (2020) assume without question that the great appendage of megacheirans must be deutocerebral, although the grounds for the argument are unclear.…”

Aquatic stem group myriapods close a gap between molecular divergence dates and the terrestrial fossil record

“…Other candidates for Cambrian myriapods, such as Xanthomyria and Pseudoiulia (31), have been associated based on having a homonymous, multisegmented trunk. At least some of these taxa can be assigned to other arthropod groups; for example, Pseudoiulia is apparently allied to jianfengiid "great appendage" arthropods (32).…”