Early Cambrian fuxianhuiids from China reveal origin of the gnathobasic protopodite in euarthropods

Euarthropods owe their evolutionary and ecological success to the morphological plasticity of their appendages. Although this variability is partly expressed in the specialization of the protopodite for a feeding function in the post-deutocerebral limbs, the origin of the former structure among Cambrian representatives remains uncertain. Here, we describe Alacaris mirabilis gen. et sp. nov. from the early Cambrian Xiaoshiba Lagerstätte in China, which reveals the proximal organization of fuxianhuiid appendages in exceptional detail. Proximally, the post-deutocerebral limbs possess an antero-posteriorly compressed protopodite with robust spines. The protopodite is attached to an endopod with more than a dozen podomeres, and an oval flap-shaped exopod. The gnathal edges of the protopodites form an axial food groove along the ventral side of the body, indicating a predatory/scavenging autecology. A cladistic analysis indicates that the fuxianhuiid protopodite represents the phylogenetically earliest occurrence of substantial proximal differentiation within stem-group Euarthropoda illuminating the origin of gnathobasic feeding.


Supplementary Note 1 | Systematic Palaeontology
Emended diagnosis. Fuxianhuiids with subtrapezoidal head shield with approximately 1:4 length/width ratio, covering three anteriormost reduced tergites. Trunk subidivided into two morphologically distinct regions, consisting of anterior limb-bearing thorax with welldeveloped expanded tergopleurae, and narrow limb-less abdomen with ring-like tergites. Endopods of biramous limbs with rounded termination; endopods short in length, not reaching beyond the thoracic tergite and head shield margins.
Remarks. The close morphological similarities shared between Fuxianhuia species 2,8,11 and Guangweicaris-particularly the presence of three reduced tergites and the differentiation of the trunk into a thoracic and abdominal regions-support their classification within Fuxianhuiidae. We follow Yang 12  Emended diagnosis. Fuxianhuiids with subtrapezoidal heart-shaped head shield with approximately 1:1 length/width ratio, covering five anteriormost reduced tergites. Trunk tergites gradually taper in width posteriorly. Biramous limbs present throughout most of trunk, except for posteriormost tergites. Endopod of biramous limbs well-developed, terminating in conical tip. Enodpods elongate, frequently reaching beyond trunk tergite and head shield margins.
Remarks. Alacaris mirabilisis confidently recognized as a member of Chengjiangocarididae Hou and Bergström 8 based on the presence of five anteriormost reduced trunk tergites, the dimensions of the head shield, a posterior tapering trunk, and the morphology of the endopods. The main differences between Alacaris and Chengjiangocaris species 2,8,13 are expressed in the number of trunk tergites and the presence of a well-developed protopodite in the former taxon.
Inapplicable for taxa lacking a distinct anterior sclerite (Character 17). An elongate anterior sclerite, compared to width, is seen in the hurdids, specifically Hurdia victoria, and Aegirocassis benmoulae, whilst the anomalocaridids, and upper-stem-group euarthropods have an anterior sclerite that is wider than long.

Tallest point of carapace.
Inapplicable for taxa lacking a carapace (Character 24). There is a lot of variety of this character amongst "carapace-bearing arthropods", with isoxyids typically possessing a shallow carapace posterior with the tallest point occurring in the anterior half of the domicilium, whist protocaridids are more rounded, with the tallest point occurring towards the middle, and fuxianhuids towards the posterior of the carapace.

Height to length ratio of carapace domiciluium.
Inapplicable for taxa lacking a carapace (Character 24). This character serves to distinguish the carapaces of most "carapace-bearing arthropods", in which the carapace is typically longer than wide, from fuxianhuids, in which the carapace is wider than long.

Length of antero-dorsal carapace spines.
Inapplicable for taxa lacking antero-dorsal carapace spines (Character 29). This character specifically refers to species of Isoxys. Both I. volucris, and I. curvirostratus possess an elongate antero-dorsal spine, whilst that of I. acutangulus and I. auritus is much shorter.

Length of postero-dorsal carapace spines.
Inapplicable for taxa lacking postero-dorsal carapace spines (Character 29). This character specifically refers to species of Isoxys.

Slope of posterior carapace margin.
Inapplicable for taxa lacking a carapace (Character 24). This character serves to distinguish Isoxys from other species of "carapace-bearing arthropods". Isoxys is unique in possessing a deeply sloped posterior carapace margin.

Meristic characters
Meristic characters were analysed as continuous characters. This differs from previous analyses that have treated them as discrete, thereby creating arbitrary bins and reducing character linkage and hindering trait determination.

Number of trunk segments.
This character could not be determined for many taxa bearing a carapace, as this feature frequently covers an anterior series of poorly sclerotized trunk segments (e.g. Nereocaris, Loricicaris). Likewise, this character was not coded for the trilobite Olenoides serratus, as the exact number of segments in the pygidium could not be determined.

Number of prothoracic segments.
This character is inapplicable for taxa lacking a prothorax (Character 42). The fuxianhuidids, namely Guangweicaris spinatus, Fuxianhuia protensa, and F. xiaoshibaensis, possess three prothoracic segments, whilst the chengjiangocaridids, Alacaris mirabilis, Chengjiangocaris longiformis, and C. kunmingensis, possess five, and Shankoia zhenghei possesses six. This character could not be adequately determined for Liangwangshania biloba as there is little variation between the morphology of the posterior prothoracic segments and the anterior post-prothoracic segments.

Number of post-prothoracic thorax segments.
This character is inapplicable for taxa lacking a prothorax (Character 42). Unfortunately, the extent of the thorax could not be determined in a number of fuxinhuids as the position of the appendage, which would serve to delineate the thorax in taxa without a posteriorly differentiated abdomen, could also not be determined. Guangweicaris spinatus possesses a short, five segmented, post-prothoracic thorax, whilst the two species of Fuxianhuia both possess 17.

Number of abdominal segments.
This character is inapplicable for taxa lacking a distinct abdomen delineated by either a lack of appendages, or a notable change in dimension from the anterior (thoracic) trunk segments.

Number of post-protocerebral cephalic appendage pairs in cephalic region.
This character is inapplicable for taxa lacking a distinct sclerotized cephalic covering, and could not be determined in most "carapace-bearing arthropods" due to uncertainty regarding the position of the cephalon-trunk boundary. In fuxianhuids this can be determined based on the position of the prothorax relative to the anterior appendages.

Number of podomeres in differentiated tritocerebral appendage.
This character is inapplicable for taxa lacking a pair of differentiated tritocerebral appendage (Character 61). All fuxianhuids for which a differentiated tritocerebral appendage is known possess three segments in each appendage, whilst megacheirans possess either five or six, and the protocaridids, Branchiocaris pretiosa and Tokumnia katalepis both possess eight.

Number of spine-bearing distal podomeres on tritocerebral appendage.
This character is inapplicable for taxa lacking spinose projections on a differentiated tritocerebral appendage (Character 61).

Number of exite segments.
This character is inapplicable for taxa lacking exites (Character 65). This character serves to distinguish advanced megacheirans, specifically Yohoia tenuis and Leanchoilia superlata, and the trilobite Olenoides serratus, which possess an exite composed of two segments, from the other megacheirans, and stem-lineage euarthropods, including the dinocaridids, and "carapace-bearing arthropods", which possess just a singular segment.