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

Abstract

BackgroundExtended 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.ResultsHere, 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1262-6) contains supplementary material, which is available to authorized users.

Developing an integrated understanding of the evolution of arthropod segmentation using fossils and evo-devo

“…It has long been known that fuxianhuiids have many more trunk appendages than tergites [91], and the discovery of the ventral nerve cord in the trunk of the fuxianhuiid Chengjiangocaris kunmingensis showed that ganglia of the nerve cord correspond to the distribution of appendages [102]. The regular, alternating pattern of terminal tergite addition and shedding of abdominal tergites into the thorax in Fuxianhuia, described above, has been interpreted as tergal formation corresponding to a general/primitive arthropod pattern versus a decoupled and phylogenetically derived mode of appendage development [82]. Fuxianhuiids are thus potentially relevant to discussion about dorsoventral decoupling in arthropods more generally [101], or lack of integration of different organ systems into one segmentation system.…”

“…The best-known example is the differentiation of the extant insect body into head, thorax and abdomen, but tagmatization is also well known from extinct groups. Fuxianhuiids, for example, have appendages on the anterior part of the trunk but have a limbless batch of segments in the posterior part of the trunk [82], analogous to the abdomen of extant arthropods (e.g. hexapods).…”

“…Ontogenetic data for fossil taxa are rare, but there are at least some cases that conform to this pattern. The ontogeny of Fuxianhuia protensa shows that tergites form at a terminal growth zone, and moults involving tergite addition alternate with ones in which a limbless abdominal segment is shed into the appendage-bearing thorax [82]. If fuxianhuiids are stem-group arthropods, as is widely accepted, an association between tagmosis (including presence versus absence of appendages on tagmata) and different modes of segment generation predates the origin of the arthropod crown-group.…”

Computed tomography sheds new light on the affinities of the enigmatic euarthropod Jianshania furcatus from the early Cambrian Chengjiang biota

“…Similar to other major Cambrian Konservat-Lagerstätten around the world [16][17][18][19][20], the metazoan community preserved in Chengjiang is dominated by euarthropods in terms of species richness and abundance, which in addition to a rich trilobite fauna also includes several dozens of non-biomineralized taxa [12,21,22]. The superb quality of soft-tissue preservation in Chengjiang fossils has produced deep insights into the biology of Cambrian euarthropods, informing about important aspects of their internal anatomy such as the digestive tract [23][24][25] and nervous system [26][27][28], as well as insights into their behavior and ecology [29][30][31]. Arguably one of the most remarkable contributions of Chengjiang euarthropods has been the availability of detailed morphological data on the ventral appendages of disparate groups that illuminate the functional morphology and higher phylogenetic affinities of these organisms [29,[32][33][34].…”

Why the term “larva” is ambiguous, or what makes a larva?

“…For Arthropoda sensu stricto, the sclerotised arthropods, the case is different. Exceptionally preserved fossils provide indication that the earliest sclerotised arthropodan species would hatch with fewer segments than the adult, adding them post‐embryonically (e.g., Fu, Ortega‐Hernández, Daley, Zhang, & Shu, and references therein; see also Waloszek & Maas, ). Hence, these immatures could be interpreted as morpho‐larvae s.l.…”