Anamorphic development and extended parental care in a 520 million-year-old stem-group euarthropod from China

Abstract

Background: Extended parental care is a complex reproductive strategy in which progenitors actively look after their offspring up to - or beyond - the first juvenile stage in order to maximize their fitness. Although the euarthropod fossil record has produced several examples of brood-care, the appearance of extended parental care within this phylum remains poorly constrained given the scarcity of developmental data for Palaeozoic stem-group representatives that would link juvenile and adult forms in an ontogenetic sequence.

Results: Here, we describe the post-embryonic growth of Fuxianhuia protensa from the early Cambrian Chengjiang Lagerstätte in South China. Our data demonstrate anamorphic post-embryonic development for F. protensa, in which new tergites were sequentially added from a posterior growth zone, the number of tergites varies from eight to 30. The growth of F. protensa is typified by the alternation between segment addition, followed by the depletion of the anteriormost abdominal segment into the thoracic region. The transformation of abdominal into thoracic tergite is demarcated by the development of laterally tergopleurae, and biramous walking legs. The new ontogeny data leads to the recognition of the rare Chengjiang euarthropod Pisinnocaris subconigera as a junior synonym of Fuxianhuia. Comparisons between different species of Fuxianhuia and with other genera within Fuxianhuiida suggest that heterochrony played a prominent role in the morphological diversification of fuxianhuiids. Functional analogy with the flexible trunk ontogeny of Cambrian and Silurian olenimorphic trilobites suggests an adaptation to sporadic low oxygen conditions in Chengjiang deposits for F. protensa. Finally, understanding the growth of F. protensa allows for the interpretation of an exceptional life assemblage consisting of a sexually mature adult alongside four ontogenetically coeval juveniles, which constitutes the oldest occurrence of extended parental care by prolonged cohabitation in the panarthropod fossil record.

Conclusions: Our findings constitute the most detailed characterization of the post-embryonic development in a soft-bodied upper stem-group euarthropod available to date. The new ontogeny data illuminates the systematics, trunk segmentation and palaeoecology of F. protensa, offers insights on the macroevolutionary processes involved in the diversification of this clade, and contributes towards an improved understanding of complex post-embryonic reproductive ecology in Cambrian euarthropods.

Keywords: Chengjiang; Fuxianhuia; Hemianamorphosis; Heterochrony; Post-embryonic development; Reproductive ecology.

Fig. 1

Ontogenetic stages of Fuxianhuia protensa from the early Cambrian Chengjiang Lagerstätte in South China. a ELI 0722A, stage 8; b) ELI 0728, stage 9; (c) ELI 0034, stage 24a; (d) ELI 0050, stage 25b; (e) ELI 0001A, stage 26b; (f) ELI 36–77, stage 27a; (g) ELI 520-27A, stage 28a; (h) ELI 0011, stage 30b. Abn, abdominal tergite; ant, antennae; asc, anterior sclerite; hs, head shield; rt., reduced anterior tergites; tf, tail flukes; Thn, thoracic tergite; wl, walking legs

Fig. 2

Trunk limb development in Fuxianhuia protensa from the early Cambrian Chengjiang Lagerstätte in South China. a CJ1069, articulated adult specimen of uncertain ontogenetic stage with dorsal exoskeleton prepared to illustrate the presence of multiple pairs of trunk appendages associated with each trunk tergite; note the morphological distinction between the limb-bearing thorax with expanded tergopleurae and the limb-less narrow abdomen. b Magnification of trunk appendages; note that endopods are less developed, smaller in size and have less podomeres towards the posterior end of the thorax. Abn, abdominal tergite; Thn, thoracic tergite; wl, walking legs

Fig. 3

Fuxianhuia protensa stages 8 and 9. a-j Stage 8; (a and b) ELI 0722A; (c and d) ELI 0723A; (e and f) ELI 0731; (g and h) ELI MU76A-c; (I and j) ELI MU76B-b; (k and l) ELI 0728, stage 9. Abn, abdominal tergite; ant, antennae; asc, anterior sclerite; hs, head shield; rt., reduced anterior tergites; SPA, specialized post-antennal appendage; tf, tail flukes; Thn, thoracic tergite; wl, walking legs

Fig. 4

Ontogenetic changes in trunk region of Fuxianhuia protensa during post-embryonic development. a Stage 8 is the earliest juvenile available, and possesses 4 thoracic limb-bearing tergites with short tergopleurae, followed by 4 limb-less cylindrical tergites. The three reduced anteriormost tergites under the head shield remain invariant. Throughout ontogenetic development, the most anterior abdominal tergite (pink) develops expanded pleurae and walking legs, transforming into the most posterior thoracic tergite (yellow). Tergite 7 arrowed in all stages for comparison. Stage 30b is the oldest known phase. b Partial trunk segmentation schedule for F. protensa; complete ontogenetic reconstruction provided in Fig. 11

Fig. 5

Fuxianhuia protensa stage 24. a and b ELI 0034, stage 24a; (c and d) ELI 0373A, stage 24b; (e and f) ELI 0373B; counterpart, stage 24b. Abn, abdominal tergite; ant, antennae; asc, anterior sclerite; hs, head shield; rt., reduced anterior tergites; SPA, specialized post-antennal appendage; tf, tail flukes; Thn, thoracic tergite; wl, walking legs

Fig. 6

Fuxianhuia protensa stage 25. a-d Stage 25a; (a and b) ELI 0469; (c and d) ELI 0591; (e-h) Stage 25b; (e and f) ELI 0076; (g and h) ELI 0050; (i and j) ELI 0276, stage 25 individual with 14 thoracic tergites and 11 abdominal tergites. Abn, abdominal tergite; ant, antennae; hs, head shield; rt., reduced anterior tergites; tf, tail flukes; Thn, thoracic tergite

Fig. 7

Fuxianhuia protensa stage 26. a and b ELI 0073, Stage 26a; (c-g) Stage 26b; (c) ELI 0006A; (d and e) ELI 0052B; (f and g) ELI 0001A. Abn, abdominal tergite; asc, anterior sclerite; hs, head shield; rt., reduced anterior tergites; tf, tail flukes; Thn, thoracic tergite

Fig. 8

Fuxianhuia protensa stage 27. a and b ELI 0073A, stage 27a; (b-g) Stage 27b; (c) ELI 0131A; (d and e) ELI 0092A; (f and g) ELI 0123B. Abn, abdominal tergite; hs, head shield; rt., reduced anterior tergites; tf, tail flukes; Thn, thoracic tergite

Fig. 9

Fuxianhuia protensa stage 28 and 29. a and b ELI 520-27A, Stage 28a; (c and d) ELI 0641, stage 28b; (e) ELI MU76A, part, stage 29; (f) ELI MU76B, counterpart, Stage 29. Abn, abdominal tergite; hs, head shield; rt., reduced anterior tergites; tf, tail flukes; Thn, thoracic tergite

Fig. 10

Fuxianhuia protensa stage 30b. a and b ELI 0011. Abn, abdominal tergite; hs, head shield; rt., reduced anterior tergites; tf, tail flukes; Thn, thoracic tergite

Fig. 11

Reconstruction of the trunk segmentation schedule of Fuxianhuia protensa. Note that stage 29a specimens have not been found

Fig. 12

Patterns of ontogenetic development in Fuxianhuia. a Ontogenetic trajectory of Fuxianhuia protensa, illustrating alternation between phases of posterior segment addition (slopes), and abdominal to thoracic tergite transformation (plateaus). Dashed lines denote unavailable ontogenetic stages. b Relationship between ontogenetic stage and body size, as expressed by thoracic length, in articulated individuals of F. protensa (n = 57) (Figs. 1, 3, 4, 5, 6, 7, 8, 9 and 10) and Fuxianhuia xiaoshibaensis (n = 4) (Additional file 1: Table S1). Note that the Y axis excludes the three reduced tergites that typify Fuxianhuia from total trunk tergite count

Fig. 13

Fossil evidence for extended parental care in Fuxianhuia protensa. a ELI MU76A-a, life assemblage including a stage 29 – most likely sexually mature – adult individual and four stage 8 juveniles. b ELI MU76B-b, counterpart, articulated stage 8 juvenile with preserved eyes. c ELI MU76A-c, articulated stage 8 juvenile with preserved gut; note the presence of reduced tergites underneath head shield (see also Fig. 3). d ELI MU76A-d, two articulated stage 8 juveniles with preserved gut and walking legs. Abbreviations: Abn, abdominal tergite; hs, head shield; tf, tail flukes; Thn, thoracic tergite; wl, walking legs

Fig. 14

Reconstruction of extended parental care in Fuxianhuia protensa