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Tiny Individuals Attached to a New Silurian Arthropod Suggest a Unique Mode of Brood Care

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Tiny Individuals Attached to a New Silurian Arthropod Suggest a Unique Mode of Brood Care Tiny individuals attached to a new Silurian arthropod suggest a unique mode of brood care Derek E. G. Briggsa,b,1, Derek J. Siveterc,d, David J. Sivetere, Mark D. Suttonf, and David Leggc aDepartment of Geology and Geophysics, Yale University, New Haven, CT 06520-8109; bYale Peabody Museum of Natural History, Yale University, New Haven, CT 06520-8109; cOxford University Museum of Natural History, Oxford OX1 3PW, United Kingdom; dDepartment of Earth Sciences, University of Oxford, Oxford OX1 3AN, United Kingdom; eDepartment of Geology, University of Leicester, Leicester LE1 7RH, United Kingdom; and fDepartment of Earth Sciences and Engineering, Imperial College London, London SW7 2BP, United Kingdom Edited by Alessandro Minelli, University of Padova, Padova, Italy, and accepted by the Editorial Board March 7, 2016 (received for review January 13, 2016) The ∼430-My-old Herefordshire, United Kingdom, Lagerstätte has Diagnosis. Features include a head shield with rostrum-like an- yielded a diversity of remarkably preserved invertebrates, many of terior projection, large uniramous antenna, chelate limb, and two which provide fundamental insights into the evolutionary history other biramous appendages in the head, the last similar to those and ecology of particular taxa. Here we report a new arthropod of the trunk; an elongated trunk with long, slender lateral spines with 10 tiny arthropods tethered to its tergites by long individual on the 11 tergites, with all trunk somites bearing limbs of which threads. The head of the host, which is covered by a shield that all but the last are biramous; and a short telson and long cerci. projects anteriorly, bears a long stout uniramous antenna and a chelate limb followed by two biramous appendages. The trunk Description. The head shield is subtriangular in dorsal view (Fig. 1 comprises 11 segments, all bearing limbs and covered by tergites A and J); the margins are incompletely preserved. The posterior with long slender lateral spines. A short telson bears long parallel area is raised medially into a broad axial ridge, which is also cerci. Our phylogenetic analysis resolves the new arthropod as a present along the length of the trunk (Fig. 1 J and K). An an- stem-group mandibulate. The evidence suggests that the tethered terior rostrum-like projection extends forward and somewhat individuals are juveniles and the association represents a complex ventrally a distance similar to the length of the rest of the head brooding behavior. Alternative possibilities—that the tethered indi- shield (Fig. 1 J and K). An apparent series of four or five short EVOLUTION viduals represent a different epizoic or parasitic arthropod—appear less likely. slender lateral spines near the base of this projection are artifacts of preservation (Fig. 1J). The sides of the head shield bear a arthropod | Silurian | brood care | juvenile | Herefordshire Lagerstätte paired series of at least four long slender spines, projecting antero-laterally and curved convex dorsally (Fig. 1J). The spines increase slightly in length from anterior to posterior and are vidence of brooding in fossil arthropods is unusual and nor- Emally confined to eggs and early juveniles: later stage juve- similar in morphology to those on the trunk tergites. A swelling niles are rarely encountered. Among the highlights described from in the axial area on the ventral side of the head, which is aligned with the attachment of appendage 3, is interpreted as a hypo- the Silurian Herefordshire Lagerstätte are ostracods preserving EARTH, ATMOSPHERIC, soft parts, including evidence of a brooding strategy that persists stome (Fig. 1 B and C). AND PLANETARY SCIENCES today: eggs and possible early juveniles are held within the space at There is no evidence of eyes. The first three head appendages the rear of the carapace (1). Here we report a new larger arthropod are morphologically differentiated, whereas the fourth appears – from the same fauna, with smaller arthropods attached to the very similar to those of the trunk (Fig. 1 B D and H). tergites by means of long threads. These smaller individuals lie Due to incomplete preservation proximally and lack of infor- within or are associated with a cuticular capsule, the largest about mation on the interior morphology of the head, it is not possible to 2 mm in length, with a gape through which the appendages determine the sequence in which the first two head appendages emerged. They preserve evidence of ∼6 pairs of appendages in insert. The relative position of antenna and chelate appendages in contrast to 15 (four of them in the head) in the adult. The evidence suggests that the attached individuals are juveniles that must have Significance added segments during the transition to an adult morphology, a strategy established in trilobites, eucrustaceans, pycnogonids, and The paper reports a remarkable arthropod from the Silurian other “Orsten” forms and in short great appendage arthropods by Herefordshire Lagerstätte of England. The fossil reveals a unique the early Cambrian (2–4). If so, the parent may be a female, al- association in an early Paleozoic arthropod involving tethering though male brood care is known in arthropods (in pycnogonids of 10 tiny individuals each by a single thread to the tergites so eggs are carried by the male, which is equipped with ovigers). that their appearance is reminiscent of kites. The evidence sug- gests that these are juveniles and that the specimen records a Results unique brooding strategy. This is part of a diversity of complex Aquilonifer spinosus is a new genus and species of arthropod from brooding behaviors in early arthropods heralding the variety the Herefordshire Lagerstätte, a late Wenlock (mid-Silurian) that occurs today. The possibility that the small individuals volcaniclastic deposit in Herefordshire, United Kingdom (5, 6). It represent a different arthropod, possibly parasitic, which colo- is preserved, as are the other fossils from this Lagerstätte, in three nized the larger individual, seems less likely. dimensions as a calcitic void fill in a carbonate concretion (7). The name of the new taxon refers to the fancied resemblance between Author contributions: D.E.G.B., Derek J. Siveter, David J. Siveter, and M.D.S. designed research; D.E.G.B., Derek J. Siveter, David J. Siveter, M.D.S., and D.L. performed research; the tethered individuals and kites, and echoes the title of the 2003 and D.E.G.B. wrote the paper with input from the other authors. novel The Kite Runner by Khaled Hosseini (aquila, eagle or kite; The authors declare no conflict of interest. -fer, suffix meaning carry; thus aquilonifer,kitebearer;spinosus, This article is a PNAS Direct Submission. A.M. is a guest editor invited by the Editorial spiny, referring to the long lateral spines on the tergites). The Board. material is a single specimen, the holotype OUMNH C.29695, 1To whom correspondence should be addressed. Email: [email protected]. registered at the Oxford University Museum of Natural History This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. (Fig. 1 and Movie S1). 1073/pnas.1600489113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1600489113 PNAS Early Edition | 1of6 Downloaded by guest on September 26, 2021 Fig. 1. Holotype of A. spinosus gen. et sp. nov., “virtual” reconstructions. (A) Dorsal view. (B) Ventral view with juveniles omitted. (C) Ventral oblique view of right head appendages and hypostome (stereo pair). (D) Ventral–oblique (stereo pair). (E) Juvenile 5, oblique view with associated capsule. (F) Juvenile 5, lateral view. (G) Lateral view with juveniles removed. (H) Anterior–oblique view (stereo pair) of posteriormost head appendage and anterior trunk ap- pendages showing exopods. (I) Proximal part of antenna showing spines (stereo pair). (J) Dorsal view without appendages (stereo pair) with juveniles numbered as referred to in text. (K) Anterodorsal–oblique view. (L) Anterior view (stereo pair). (M) Dorsal view of posterior of trunk (stereo pair). (N)Anterior view of trunk limb 9 (stereo pair). ap, juvenile appendages; b, basis; c, claw; ca, capsule; e, endopod; g, gut; h1–4, head appendages; hy, hypostome; t, telson; t1–11, trunk appendages; x, exopod. Numbers refer to trunk tergites, attached juveniles, or appendage podomeres as appropriate. (Scale bars, 1 mm.) other Paleozoic arthropods, however, suggests that the uniramous enumerate—neither spines nor podomere boundaries are evi- nonchelate appendage (the antenna) is anteriormost (8). dent more distally. Spine bases are evident on the left appendage Head appendage 1 (green; Fig. 1 A, B, D, G, I, and K), as but not the spines themselves. Extrapolation suggests that the designated here, is uniramous, antenniform, and large. The right total number of podomeres is about 25. This first appendage is appendage is the better preserved (the reconstruction of the left about the same length as the body, including the “rostrum” but is incomplete distally). The angle of the slices (see Methods), excluding the cerci. subparallel to the length of the appendage, makes the proximal Head appendage 2 (pink; Fig. 1 A–D, K, and L) extends for- part difficult to interpret, but it may consist of three or four ward but not beyond the anterior projection of the head shield. segments similar in length to the more distal ones or, perhaps Subtle changes in direction along the length of the right limb less likely, a long basal segment. The appendage tapers gradually to a point. The individual podomeres are narrower proximally suggest that there may be as many as five proximal podomeres, and expand distally (Fig. 1I) to a point about their midlength but this is not certain (the slices run along the length of the limb, where they bear two short narrow spines, which project dorso- rather than transverse to it, obscuring details). The appendage laterally relative to the orientation of the trunk; more spines may terminates in a laterally directed swollen chela-like structure, have been present.
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