- Research article
- Open Access
Anamorphic development and extended parental care in a 520 million-year-old stem-group euarthropod from China
© The Author(s). 2018
- Received: 8 April 2018
- Accepted: 20 September 2018
- Published: 29 September 2018
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.
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.
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.
- Post-embryonic development
- Reproductive ecology
Fuxianhuiida represents a distinctive clade of upper stem-group euarthropods exclusively known from the early Cambrian of South China [1–4], and figure among the most thoroughly scrutinized Lower Palaeozoic taxa owing to several remarkable instances of soft-tissue preservation [5–11]. Despite their contribution towards understanding the origin of Euarthropoda [1–11], basic aspects of the post-embryonic development of fuxianhuiids and most other stem lineage representatives remain largely uncharted . Although it has been recognized that fuxianhuiid populations include individuals of different sizes and variable number of exoskeletal trunk tergites suggesting the occurrence of different ontogenetic stages [1–3, 5], there is no formal description of this variability nor its implications for the palaeobiology of these animals. Some studies have produced remarkable insights on the post-embryonic development in other Cambrian stem-group euarthropods, such as the recognition of limb rudiments in a larva of the megacheiran Leanchoilia illecebrosa , and the changes in bivalved carapace morphology and body segment count during growth in Isoxys auritus . However, detailed information on the ontogeny and reproduction of Lower Palaeozoic euarthropods is for the most part only available from crown-group members [15–25], precluding the ancestral reconstruction of these traits during the early evolution of the phylum. Here we describe the post-embryonic development of Fuxianhuia protensa from the Cambrian (Stage 3) Chengjiang biota in South China [1, 5]. This represents the most comprehensive characterization of the ontogeny in a stem-group euarthropod to date, and leads to the recognition of parental care in fuxianhuiids, casting new light on the complex reproductive behaviour of early animals during the Cambrian Explosion.
Morphometric data obtained from previously published and our newly documented specimens of F. protensa indicate that overall body size (estimated from thoracic sagittal length) is positively correlated with the number of trunk tergites, and that there is a substantial degree of body size variation among later ontogenetic stages (Fig. 12b). This is partly owing to changes in the proportions of the dorsal exoskeleton throughout ontogeny, which complicate morphometric measurements of overall body size. For example, some of the stage 8 or 9 individuals have a similar thoracic length to that of stage 24 specimens (Fig. 12b). This can be explained by the difference in trunk tergite proportions between instars, as stage 8 and 9 individuals have proportionately elongate thoracic tergites, whereas the thoracic tergites of Stage 24 are relatively shorter and wider. The considerable overlap in size between different ontogenetic stages may also be a consequence of natural size variation between populations of specimens pooled together from several different localities within the Yu’anshan Member of the Chiungchussu Formation (Additional file 1: Table S1). Given that body size in extant euarthropods is a multifaceted phenomenon that is affected by both intrinsic and extrinsic factors , it is possible that environmental variables spanning short periods of geological time, such as local shifts in nutrient availability or temperature acting anywhere from annual seasons to centuries, could affect the rate of growth and maximum body size within the studied F. protensa populations. These differences could also be partly attributed to sexual dimorphism. However, discerning (at least some of) the primary effects responsible for controlling body size in F. protensa will only become possible through the additional input of completely articulated specimens corresponding to early juvenile stages.
The ontogenetic development of Fuxianhuia protensa
The new data on F. protensa represents the first detailed characterization of the post-embryonic development in an upper stem-group euarthropod [10, 12]. Despite the gap in the ontogenetic series between stage 9 and stage 24 (Fig. 11a; Fig. 12), the smaller individuals can be reliably identified as representatives of F. protensa based on their shared morphological features. The presence of stalked eyes connected to an anterior sclerite, ventral antennae, a pair of specialized post-antennal appendages, limb polypody, and a loosely attached head shield that covers multiple reduced anterior tergites are collectively strong indicators of fuxianhuiid affinities (Fig. 1a, b; Fig. 3) [1–5, 9, 11]. The dorsal exoskeleton of stages 8 and 9 resembles Chengjiangocaris [1, 2] and Alacaris  in the absence of a differentiated thoracic and abdominal regions; however, the possession of only three reduced anteriormost tergites underneath the head shield represents a key feature of Fuxianhuia [1, 2, 5, 11, 29], whereas most other genera of Fuxianhuiida possess five [1, 2, 29] or six  reduced tergites. Although the presence of three reduced tergites is also known in Guangweicaris spinatus from the Guanshan biota (Cambrian Stage 4, Wulongqing Formation) , this taxon has never been reported from any of the stratigraphically older Chengjiang localities despite substantial collecting efforts on the Chiungchussu Formation [1, 5, 6, 8, 11, 27, 30], and thus it is highly unlikely that the juvenile specimens are linked to it. In this context, the differences in the relative size and shape of the thoracic tergites between the F. protensa juveniles and adult specimens reflect ontogenetic change, as demonstrated by the gradual broadening of the thoracic tegites during stages 24 and 25 (Fig. 1a-d; Figs 3, 4, 5 and 6).
The ontogeny of F. protensa indicates that this taxon underwent anamorphic post-embryonic development (Figs. 4, 12, 13), in which new tergites were added sequentially from a posterior growth zone [19, 20, 24, 31, 32]. The biphasic developmental pattern of F. protensa is reminiscent of euarthropods that possess morphologically regionalized trunk regions, such as trilobites [24, 31, 32] and some crustaceans [21, 33, 34]. Trilobite development is broadly characterized as hemianamorphic; it consists of an anamorphic phase in which new segments are added from a posterior growth zone after each moult (accumulation), followed by an epimorphic phase with a fixed number of segments, which may involve their release from the fused pygidium into the freely articulating thorax (depletion), or a body size increase without significant morphological changes [24, 31, 32, 35]. Although the mode of ontogenetic growth is somewhat variable between different trilobite taxa , the biphasic growth of F. protensa bears some broad similarities with that of Shumardia (Conophyrs) salopiensis [24, 36]; both are typified by the alternation between posterior addition of segments, followed by the release of the anteriormost pygidial/abdominal segment into the thoracic region. Specifically, the pygidium of S. salopiensis alternates between three or four segments through part of its meraspid stage [24, 36], and thus superficially resembles the development of F. protensa in which the abdomen count varies between 12 and 13 tergites.
The growth trajectory of F. protensa as recorded by the morphometric data (Fig. 12b) also evokes parallels with that of the intensively studied Silurian proetid trilobite Aulacopleura konincki. Here, the range of body size is somewhat constrained among juvenile stages (meraspids), but becomes much more variable during late ontogeny resulting in mature adults (holaspids) with a polymorphic trunk segment count [37, 38]. The prevailing interpretation for the growth pattern of A. konincki favours a developmental model where the total number of thoracic segments was determined during early ontogeny, and once this maximum was reached, growth continued epimorphically in the holaspid stage. The small sample size of measurable juveniles available for F. protensa (stages 8 and 9, n = 9; Additional file 1: Table S1) prevents us from drawing comparable interpretations to those of A. konincki for the precise regulatory mechanisms responsible for trunk development (e.g. ontogenetically early versus late patterning, see ref. [37, 38]). However, the similar variability in body size relative to ontogenetic stage observed in late growth stages of F. protensa (Fig. 12b; trunk tergites versus thoracic length) and also holaspids of A. konincki (see fig. 3 in ref. ; thoracic tergites versus cranidial centroid size) suggests the existence of an epimorphic phase in the former fuxianhuiid. In this case, F. protensa growth would correspond to hemianamorphosis, as is also observed in numerous Cambrian euarthropods [12, 13, 19, 20, 24, 37, 38]. Although a definitive growth model is difficult to determine owing to the incompleteness of the early ontogenetic trajectory of F. protensa, the occurrence of hemianamorphic development in this taxon is in accord with most accepted interpretations for the ancestral mode of growth for crown-group Euarthropoda [19, 21, 24], as also suggested by the phylogenetic position of fuxianhuiids [9, 10, 12, 29]. Comparisons between the ontogenetic trajectories of F. protensa and A. konincki also raise the possibility that the former may have also exhibited adult polymorphism. Holaspids of A. konincki express five distinct morphotypes that possess between 18 and 22 freely articulating thoracic tergites, as well as a pygidium with three to seven segments [37, 38]. The five adult morphotypes of A. konincki correspond to the ontogenetic stages that show a substantial body size variation (estimated by cranidial centroid size) compared to the meraspids, namely those that have between 18 to 22 thoracic tergites (see fig. 3 in ref. ). When contrasted with the body size variation observed throughout development in F. protensa (Fig. 12b), the same parameter would suggest that this taxon may also possess multiple morphotypes, which would at least encompass stages 26 to 30. However, the full implications of this interpretation are yet again limited by the scarcity of juvenile F. protensa material that would inform on the entire growth trajectory, and the mixed provenance of the fossils from several localities (Additional file 1: Table S1).
Among extant euarthropods, the biphasic development of the dorsal exoskeleton in F. protensa evokes comparison with that of Cephalocarida, a relatively poorly understood but highly ecologically specialized clade of meiofaunal pancrustaceans [33, 34, 39]. The post-cephalic exoskeleton of cephalocarids comprises a limb-bearing thorax with pivot-jointed tergites that possess laterally extended tergopleurae, followed by an elongate and flexible abdomen formed by cylindrical tergites without appendages. During their early anamorphic development, the trunk of cephalocarids alternates between the production of new abdominal segments from a posterior growth-zone, and the transformation of the anteriormost abdominal tergite into a limb-bearing thoracic tergite with expanded tergopleurae [33, 34]. Although there is some variation on the timing of these events between cephalocarid species , this biphasic pattern resembles the ontogenetic development of the trunk in F. protensa (Figs. 4, 12, 13). The peculiar development of Cephalocarida has been considered as autapomorphic among crustaceans , which suggests that the growth mode of F. protensa most likely evolved independently given the phylogenetic position of Fuxianhuiida within the euarthropod stem lineage [10–12, 29]. This interpretation is further supported by the lack of substantial dorsal exoskeletal tagmosis in closely related taxa such as Chengjiangocaris [1, 5], Liangwangshania [3, 40] and Alacaris . Ultimately, the ontogeny and phylogenetic position of F. protensa support anamorphosis – and particularly hemianamorphosis – as the ancestral mode of euarthropod post-embryonic development [12, 13, 18–21, 24], whereas the dorsal exoskeletal tagmosis of Fuxianhuia species [1, 2, 5] - and the closely related Guangweicaris  - are best regarded as a derived condition within upper stem-group Euarthropoda [10–12, 29].
Our data also offer additional insights into the segmental organization of fuxianhuiids. It is well established that the thoracic tergites of F. protensa bear more than one set of biramous limbs, which raises the question of whether this type of segmental mismatch results from the derived organization of the dorsal or ventral side of the trunk [1, 2, 5, 9, 41]. The formation of the tergites from the posterior growth zone in the abdomen (Figs. 4, 11, 12), together with their release into the thoracic region and subsequent lateral expansion of the tergopleurae, suggest that the dorsal exoskeleton of fuxianhuiids follows the conventional pattern of segment production observed in most euarthropods [19–22, 31, 32, 35]. This condition implies that the presence of multiple leg pairs associated with each thoracic tergite most likely represents a derived mode of ventral segmentation exclusive to this body region, further supported by the recent discovery of metamerically arranged midgut diverticulae in F. protensa that match the dorsal segmentation pattern . Although rare, a similar type of dorsoventral segmental mismatch is also observed in the ventral trunk of the branchiopod Triops cancriformis [42, 43]. The anamorphic growth of T. cancriformis comprises the formation of limb-less abdominal segments from a posterior growth zone, which then develop between three and four pairs of limb buds that result in supernumerary thoracopods per segment in the adult . This condition is closely reminiscent to that of F. protensa, including the fact that the newly formed posterior thoracic appendages are less developed compared to those on the anterior end of the body (Fig. 2).
Pisinnocaris as junior synonym of Fuxianhuia
The new data on the ontogenetic development of F. protensa has direct implications for the diversity of fuxianhuiids from Chengjiang-type biotas in South China. Juveniles corresponding to stages 8 and 9 (Fig. 1a,b; Fig. 3) closely resemble the enigmatic euarthropod Pisinnocaris subconigera . Pisinnocaris is only known from few specimens that reach a maximum length of 10.7 mm, and thus falls within the size range of stage 8 juveniles of F. protensa (Figs. 3, 4, 11, 12). The morphology of Pisinnocaris consists of a pair of stalked eyes followed by uniramous antennae, a subtrapezoidal head shield, and a trunk composed of at least 8 or 9 tergites that tapper in width posteriorly. The type material does not preserve walking legs, but shows traces of possible attachment sites that suggest the presence of several limb pairs per tergite. It is possible to subdivide the trunk into a thoracic region based on the presence of short tergopleural spines, whereas these are absent on the comparatively more narrow abdominal tergites . Although the available material of Pisinnocaris from the Chengjiang does not demonstrate the presence of reduced anterior tergites underneath the head shield as observed in juveniles of F. protensa (Fig. 3), all other aspects of the exoskeletal organization are identical between these taxa. Furthermore, Zeng et al.  recently illustrated a single specimen of a small (ca. 6 mm long) euarthropod tentatively assigned to Pisinnocaris based on the morphology of the head shield and anterior trunk region from the Cambrian (Stage 3) Hongjinshao Formation at Chenggong. This specimen is highly significant, as it unequivocally demonstrates the presence of reduced anterior tergites underneath the head shield, and traces of multiple limbs associated with the thoracic tergites. Although the posterior half of the Chenggong euarthropod is not preserved, its morphology and size fit comfortably within those of stage 8 or 9 juveniles of F. protensa (Figs. 3, 4, 11, 12). Collectively, these observations indicate that Pisinnocaris actually corresponds to a juvenile of Fuxianhuia, rather than a separate taxon; thus, Pisinnocaris is best regarded as a junior synonym of Fuxianhuia.
Xu  described a single Chengjiang euarthropod specimen as Pisinnocaris sp. based on the morphology of the head shield and similar trunk organization. Although Pisinnocaris sp. could be of potential relevance to the present study given the possession of 11 trunk tergites, the single specimen does not demonstrate the presence of reduced tergites, nor the morphological differentiation of the trunk into a thoracic and abdominal region. The trunk tappers in width posteriorly, but clearly features well-developed posterior-facing tergopleural spines throughout the entire length of the body (see Plate 1, figure 3 in ). Pisinnocaris sp. also differs from F. protensa early juveniles in having an elongate and robust tailspine with a subrectangular outline, and no evidence of the commonly preserved tail flukes (Figs. 3, 4, 5, 6, 7, 8, 9 and 10). More critically, the only known specimen of Pisinnocaris sp. reaches a body length of 47 mm, making it more than three times larger than known juveniles of F. protensa (ca. 15 mm max. length). In this context, the overall exoskeletal dorsal morphology and size of Pisinnocaris sp. most closely resemble those of the aglaspidid euarthropod Tremaglaspis [46–48], potentially extending the stratigraphic range of this taxon to the Cambrian Stage 3. Given the rarity of Pisinnocaris sp. within the Chengjiang, we refrain from formalizing this interpretation until more specimens of this problematic taxon become available for study and comparison with the type material of Tremaglaspis.
The post-embryonic ontogeny of F. protensa is characterized by the addition of tergites from a posterior growth-zone, as well as the corresponding increase in size (Figs. 4, 11, 12). Comparisons between body size increments and the number of trunk tergites reveal a substantial degree of variability in F. protensa, and indicate that there is not a simple or direct correlation between these parameters during ontogeny (Fig. 12b). This pattern resembles the flexible thoracic segmentation observed in some Cambrian olenimorphic trilobites – which are characterized by having narrow axis, extended terpleurae and segment-rich thorax – as well as the Silurian trilobite A. konincki [37, 38, 49–51]. The flexibility in adult segment number observed in olenimorphic trilobites suggests that the variable trunk segmentation of F. protensa could potentially represent an adaptation for environmental conditions with reduced oxygen, in which the presence of numerous pairs of walking legs – and their corresponding flap-like exopods – would maximize ventilation for respiration [51, 52]. Geochemical data  and the scarcity of trace fossils in these deposits , which indicate that the Chengjiang environment would have experienced fluctuating oxygen levels, offers some support to the adaptive value of flexible patterns of trunk segmentation and polypody in F. protensa by analogy with Cambrian and Silurian olenimorphic trilobites [37, 38, 51].
Morphological diversification and heterochrony in fuxianhuiid evolution
The growth pattern of F. protensa allows further comparisons with the congeneric – and stratigraphically younger – F. xiaoshibaensis [2, 29, 44]. Despite their close morphological similarities, F. xiaoshibaensis differs from F. protensa in the higher trunk tergite count, more specifically in the presence of up to 17 thoracic and 16 abdominal tergites. Although the higher tergite count of F. xiaoshibaensis could be explained as a result of continued development in F. protensa, the ontogenetic trajectories of these taxa argue against this interpretation (Fig. 12b). Individuals of F. xiaoshibaensis are up to three times smaller compared to advanced ontogenetic stages of F. protensa; these differences suggest an accelerated rate of tergite addition during early ontogeny in F. xiaoshibaensis relative to the stratigraphically older F. protensa, and fall in accordance to peramorphic heterochronic development [54–56]. This phenomenon is clearly expressed in the presence of 16 abdominal tergites of F. xiaoshibaensis, compared to the 12 – or exceptionally 13 – abdominal tergites of F. protensa, despite both species having a comparable maximum number of thoracic tergites. However, the restricted number of completely articulated specimens of F. xiaoshibaensis precludes further investigations on this matter (Fig. 12b), and thus this hypothesis awaits corroboration through the analysis of additional material.
Extended parental care in Fuxianhuia
Our survey of completely articulated specimens of F. protensa from the early Cambrian Chengjiang cast new light on several aspects of the post-embryonic ontogenetic development, palaeobiology, and reproductive behaviour of these important upper stem-group euarthropods. The recognition of anamorphosis – and likely hemianamorphosis – in F. protensa provide a minimum constrain for the origin of this ancestral growth mode for the euarthropod stem lineage. However, these findings also demonstrate that phylogenetically early diverging euarthropods already possessed a substantial degree of developmental variability, expressed in F. protensa in the biphasic pattern of tergite addition from a posterior growth zone, and the available evidence suggesting polymorphism in the number of adult thoracic tergites. Although there is still much to learn about the development of stem group euarthropods, the new data on F. protensa fills a critical gap in our understanding of the evolution of post-embryonic ontogeny, and highlights the significance of development as a tool for a more holistic understanding of the palaeobiology of extinct organisms.
The studied fossils are the result of decades of collecting effort from various localities of the Cambrian (Stage 3; locally Qiongzhusian) Yu’anshan Member of the Chiungchussu Formation of the Kunming region in South China . The material is deposited in the Early Life Institute (ELI), Northwest University, Xi’an (see Additional file 1: Table S1). Specimens were prepared with fine needles under high magnification using stereomicroscopes. Fossils were photographed with a Canon EOS 5D Mark II digital camera and were processed in Adobe Photoshop CS 5. Camera lucida and interpretative drawings were made using a Leica M80 microscope and prepared with Corel Draw X5. Morphometric data were measured from specimen digital photographs using the software FIJI .
We thank Meirong Cheng, Juanping Zhai and Yu Wu at the Early Life Institute for help during fieldwork and technical assistance. Nigel Hughes (University of California, Riverside) provided useful discussions and comments on an earlier version of the manuscript. We are grateful for comments from Joanna Wolfe and an anonymous reviewer, which helped us improve the manuscript.
This research was supported by funds from the National Key Research and Development Program (Grant No. 2017YFC0603101), Natural Science Foundation of China (Grant nos. 41621003, 41720104002, 41772011 and zhongdaxiangmu etc.), the Strategic Priority Research Program of Chinese Academy of Sciences (Grant No. XDB26000000), and 111 Project (D17013), and a Herchel Smith Research Fellowship in Biological Sciences held at the Department of Zoology and Emmanuel College at the University of Cambridge (JO-H).
Availability of data and materials
The material is deposited in the Early Life Institute (ELI), Northwest University, Xian, China. The dataset and figures supporting this article have been uploaded as part of the supplementary material.
DJF, JO-H and ACD performed research, wrote the paper and prepared the figures with input from the other authors. DJF, XLZ designed the project with input of all authors. All authors discussed and approved the manuscript.
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