Eyes and Claws Reveal the Evolution of Divergent Ecological Roles in Giant

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Palaeontology All the better to see you with: eyes and rsbl.royalsocietypublishing.org claws reveal the evolution of divergent ecological roles in giant pterygotid eurypterids Research 1 1 2 Cite this article: McCoy VE, Lamsdell JC, Victoria E. McCoy , James C. Lamsdell , Markus Poschmann , Poschmann M, Anderson RP, Briggs DEG. 2015 Ross P. Anderson1 and Derek E. G. Briggs1,3 All the better to see you with: eyes and claws 1 reveal the evolution of divergent ecological Department of Geology and Geophysics, Yale University, 210 Whitney Avenue, New Haven, CT 06511, USA 2Referat Erdgeschichte, Direktion Landesarcha¨ologie, Generaldirektion Kulturelles Erbe RLP, Große Langgasse 29, roles in giant pterygotid eurypterids. Biol. Lett. 55116 Mainz, Germany 11: 20150564. 3Yale Peabody Museum of Natural History, 170 Whitney Avenue, New Haven, CT 06520, USA http://dx.doi.org/10.1098/rsbl.2015.0564 Pterygotid eurypterids have traditionally been interpreted as active, high-level, visual predators; however, recent studies of the visual system and cheliceral morphology of the pterygotid Acutiramus contradict this interpretation. Received: 30 June 2015 Here, we report similar analyses of the pterygotids Erettopterus, Jaekelopterus Accepted: 29 July 2015 and Pterygotus, and the pterygotid sister taxon Slimonia. Representative species of all these genera have more acute vision than A. cummingsi. The visual systems of Jaekelopterus rhenaniae and Pterygotus anglicus are comparable to that of modern predatory arthropods. All species of Jaekelopterus and Pterygotus have robust crushing chelicerae, morphologically distinct from the weaker sli- Subject Areas: cing chelicerae of Acutiramus. Vision in Erettopterus osiliensis and Slimonia palaeontology acuminata is more acute than in Acutiramus cummingsi, but not to the same degree as in modern active predators, and the morphology of the chelicerae Keywords: in these genera suggests a grasping function. The pterygotids evolved with a shift in ecology from generalized feeder to specialized predator. Pterygotid pterygotid, eurypterid, arthropod vision, eurypterids share a characteristic morphology but, although some were top chelicerae, predation predators, their ecology differs radically between genera.

Author for correspondence: Victoria E. McCoy 1. Background e-mail: [email protected] Pterygotid eurypterids are large, cosmopolitan aquatic chelicerates known from the Silurian to the Devonian. Characterized by their large body size, huge for- wardly directed chelicerae and large eyes, pterygotids have traditionally been interpreted as active, high-level, visual predators [1–3]. Recent studies of the pterygotid Acutiramus, however, revealed eyes with low visual acuity inconsist- ent with the lifestyle of an active predator [4] and weak chelicerae incapable of puncturing thick cuticle or grappling with struggling prey [5], contradicting this interpretation. Here, we expand this analysis to other pterygotid genera to determine whether the conclusions drawn from Acutiramus apply to this clade as a whole.

2. Material and methods Visual acuity is primarily determined by two parameters: the number of lenses and the interommatidial angle (IOA, the angle between the optical axes of adjacent Electronic supplementary material is available lenses) [6,7]. The IOA, in particular, distinguishes active arthropod predators at http://dx.doi.org/10.1098/rsbl.2015.0564 or today from those with other ecological roles [7], and has been used to assess the visual system of fossil arthropods [4,8]. These two parameters were measured on via http://rsbl.royalsocietypublishing.org. four species of eurypterids (table 1): the pterygotids E. osiliensis, Jaekelopterus

Table 1. Data on the visual system of pterygotids and pterygotid relatives. Italicized values indicate average values. The value for Pterygotus anglicus is based 2 on a single specimen; the values for all other species were taken from multiple specimens. Values for Eurypterus sp. and Acutiramus cummingsi were taken rsbl.royalsocietypublishing.org from previously published data [4].

specimen number age formation eye area (mm2) no. lenses IOA

Erettopterus osiliensis YPMa 325005 Upper Silurian Rootsikula 309.33 4392 1.14 Erettopterus osiliensis NHMb I 2953 Upper Silurian Rootsikula 195.82 3765 1.31 average 252.57 4079 1.23 Jaekelopterus rhenaniae PWLc 2015/5308-LS Lower Devonian Odenspiel 949.20 2958 0.76

Jaekelopterus rhenaniae PWL 2004/5055-LS Lower Devonian Klerf 9.60 3362 0.95 Lett. Biol. average 479.40 3160 0.85

Slimonia acuminata YPM 33437 Upper Silurian Lesmahagow 61.19 4744 1.59 11

Slimonia acuminata NHM In 61508 Upper Silurian Lesmahagow 55.73 3405 1.44 20150564 : average 58.46 4075 1.52 Pterygotus anglicus NBMGd 10000 Lower Devonian Campbellton 590.53 4303 0.77 aYale Peabody Museum, USA. bNatural History Museum, UK. cLandessammlung fu¨r Naturkunde Rheinland-Pfalz, Mainz, Germany. dNew Brunswick Museum, Canada.

rhenaniae and Pterygotus anglicus, and the pterygotid sister taxon fall within the range (,18) indicative of active, high level Slimonia acuminata (figure 1a and the electronic supplementary predators among modern arthropods (figure 2 and table 1) material). These data were compared with previously published [7]. The evidence indicates that these eurypterids were data for the pterygotid Acutiramus cummingsi and for Eurypterus active, visual predators. sp., a more basal eurypterid typifying the plesiomorphic general- The second group includes the mid-sized (,1m ist morphology [4]. long [2,15]) S. acuminata and Erettopterus species, as well as The morphology of pterygotid chelicerae has been used as Eurypterus remipes. The chelicerae of S. acuminata are small evidence of feeding habit [9,10]. Cheliceral morphology is known in 14 eurypterid species, including the six for which with no denticles, similar to the typical eurypterid grasping vision can be analysed. The morphology of the chelicerae was appendages in E. remipes [16]. The chelicerae of Erettopterus subjected to a principal coordinates analysis (PCO) of discrete are enlarged, sometimes with differentiated denticles and characters (electronic supplementary material) and plotted in paired distal teeth that occlude completely, suggesting multidimensional space (figure 1b); no a priori assumptions that these chelicerae were also used for grasping rather were made about the function of specific morphologies. Phylo- than more specialized feeding [9]. Slimonia acuminata and genetic analysis of the pterygotoidea was performed using a E. osiliensis both have high visual acuity with an IOA between modified version of the Lamsdell & Selden matrix [11] (see the 2 and 3, and a large number of lenses. Although the number electronic supplementary material). of lenses is comparable to that in Jaekelopterus and Pterygotus, the IOA values are higher (table 1) [7]. Thus, the evidence indicates that, although this second group was predatory, Sli- monia and Erettopterus were not as highly specialized or active 3. Results and discussion as Jaekelopterus and Pterygotus. In terms of its visual system, Cheliceral morphology separates the species into three dis- Eurypterus does not cluster with Slimonia and Erettopterus, tinct groups (figure 1b), which are also differentiated on the but falls between this group and the active predatory group basis of visual acuity (IOA plotted against number of of Jaekelopterus and Pterygotus, suggesting an intermediate lenses), with the exception of the position of Eurypterus visual capability. (figure 2a). The large (up to 2 m long [2]) Acutiramus species form a The first group includes the large (up to 2.5 m long [1,2]) third group which falls farther from the other two in both Jaekelopterus and Pterygotus species, and a specimen repre- plots (figures 1b and 2a ). The chelicerae of all Acutiramus senting a new genus and species, IVPP-14593. Both species are large with differentiated denticles, including J. rhenaniae and P. anglicus have high visual acuity as indi- one which is long, strongly inclined and serrated on the cated by low IOA and a large number of lenses (figure 2 fixed ramus, suggesting a shearing or slicing function [5,9]. and table 1). The chelicerae of all studied species of Jaekelop- Acutiramus cummingsi has relatively low visual acuity, terus, Pterygotus and IVPP-14593 are enlarged and robust with few lenses and high IOA [4]. The separation of the with prominent, differentiated denticles and a curved free Acutiramus species from other pterygotids, on the basis of ramus, features associated with strong grasping and punctur- their visual system and cheliceral morphology, indicates a ing abilities in modern crustaceans [12] and scorpions [13]. distinct ecology that involved less active predation. Puncture wounds on the dorsal shield of a poraspid agnathan The variation in IOA values within A. cummingsi is due to from the Devonian of Utah have been attributed to the cheli- changes during growth: vision is less acute in the larger cera of Jaekelopterus howelli [14]. The IOA values for this group specimens [4]. This is in contrast to J. rhenaniae, in which Downloaded from http://rsbl.royalsocietypublishing.org/ on August 19, 2015

(a) 440 430 420 410 400 390 380 370 360 increased sampling of visual field 3 rsbl.royalsocietypublishing.org Silurian Devonian Acutiramus cummingsi Llandov W PLLo Ems Ei Gi Fras Famenn 3 Eurypterus remipes Eurypterus sp. Slimonia acuminata Ciurcopterus ventricosus Erettopterus osiliensis Erettopterus serricaudatus Erettopterus bilobus Jaekelopterus rhenaniae Erettopterus osiliensis Slimonia acuminata Erettopterus waylandsmithi Pterygotus barrandei Pterygotus anglicus Pterygotus anglicus 2 IVPP-I4593 Acutiramus cummingsi

Acutiramus macrophthalmus Lett. Biol. Acutiramus bohemicus Jaekelopterus rhenaniae Jaekelopterus howelli 11

(b) interommatidial angle 1.0 P. barrandei 1 20150564 : Er. waylandsmithi P. anglicus Er. bilobus 0.5 J. howelli Er. osiliensis E. remipes IVPP-I4593 J. rhenaniae Er. serricaudatus modern high-level 0 S. acuminata predatory arthropods

−0.5 1000 3000 5000 no. lenses

−1.0 Figure 2. The visual systems of Jaekelopterus rhenaniae, Pterygotus anglicus,

principal coordinate 2 Slimonia acuminata, Erettopterus osiliensis, Eurypterus sp. and Acutiramus cummingsi. Interommatidial angle (IOA) versus number of lenses, which indi- −1.5 A. cummingsi cates visual acuity; the pink shading indicates IOA values in modern active A. macrophthalmus predatory arthropods. (Online version in colour.) −2.0 A. bohemicus −1.0 0 1.0 2.0 3.0 scavenger upon soft-bodied organisms, possibly feeding in principal coordinate 1 low-light conditions or at night [4]. Figure 1. Phylogeny and cheliceral morphology of pterygotid eurypterids. Older assessments of the ecological role of the giant ptery- (a) Phylogeny of pterygotids and their relatives. (b) PCO of pterygotid che- gotid eurypterids lumped them together as high-level liceral claw morphology, the pink shading indicates IOA values as in figure 2a. predators on the basis of their general morphology [17]. Circles represent taxa for which eye data are known, hexagons taxa for which Our new data on their visual system [4] and chelicerae no eye data are available. A version of the phylogenetic tree with branch sup- yield a more detailed understanding of their lifestyles. port values is included in the supplementary material with the character lists Despite the morphological similarities between pterygotid and data matrices for the phylogenetic and principal coordinate analyses. species, their ecological roles range from a more generalized (Online version in colour.) strategy in more basal eurypterids (Erettopterus), to high- level active predation (Jaekelopterus, Pterygotus and IVPP- 14593) and specialized ambush predation or scavenging, vision is less acute in the smaller specimen (table 1 and perhaps in low light (Acutiramus). figure 2). Therefore, the pterygotids may be more similar Previous studies [5,9] on the ecological role of pterygotids in visual capacity early in their ontogeny, with specialized have been driven, in part, by debates on clade selection morphology developing later. [18,19] and clade interaction, primarily via competitive repla- The changes in pterygotid ecology associated with their cement [20,21]. Competitive replacement has been suggested evolution can be reconstructed by considering the results of to have played a role in the evolution of eurypterids and this study in a phylogenetic context (figure 1a). Erettopterus, jawless fish [17] but this hypothesis has been largely dis- in contrast to Slimonia, has the enlarged chelicerae character- missed [22]. Despite the fact that biotic competition is now istic of pterygotids, but it lacks the giant body size or generally considered to play a relatively minor role in taxon advanced visual system of Pterygotus and Jaekelopterus. survivorship [23], the possibility of competition between eur- The ancestor of Pterygotus, Jaekelopterus and Acutiramus ypterids and early vertebrates has seen a resurgence in recent developed giant body size, specialized chelicerae and an literature [1–3,24–26], alongside a debate about whether advanced visual system along with a predatory lifestyle, higher taxa (i.e. clades) exhibit distinct ecological properties as indicated by the acute vision and strong puncturing or [27–29]. Our results show that, even within clades with a dis- crushing chelicerae in Pterygotus and Jaekelopterus,andthe tinct general morphology, the ecology of constituent species similar chelicerae in IVPP-14593. These adaptations to can vary: detailed analysis is needed before ascribing a gen- active predation, except for large body size, were sub- eral ecology to a group in toto. This, in turn, supports sequently lost or secondarily modified in Acutiramus, previous conclusions [30] that pterygotids were not uni- which has very different chelicerae [10] and a weaker formly giant active predators, comprising a clade that was visual system [4], and was likely an ambush predator or outcompeted by early vertebrates. Downloaded from http://rsbl.royalsocietypublishing.org/ on August 19, 2015

Author contributions. V.E.M., J.C.L., R.P.A. and D.E.G.B. designed the study; award. R.P.A. was supported by the NASA Earth and Space Science 4 V.E.M. coordinated the research, analysed the visual systems and drafted Fellowship Programme (grant no. NNX14AP10H). the paper; J.C.L. analysed chelicera morphometrics and eurypterid phy- Acknowledgements. S. Butts and J. Utrup of the Yale Peabody Museum rsbl.royalsocietypublishing.org logeny; M.P. and R.P.A. identified and photographed specimens. All of Natural History facilitated access to specimens from the collec- authors interpreted data, edited the paper and approved the final version. tion kindly donated by S. J. Ciurca. C. Mellish at the Natural Competing interests. We have no competing interests. History Museum, London facilitated access to specimens which Funding. TNT was made available with the sponsorship of the Willi H. Taylor photographed. R. Miller provided images of Pterygotus Hennig Society. V.E.M. was supported by a National Science Foun- anglicus. We are grateful to two anonymous reviewers for com- dation Graduate Research Fellowship and a Kennedy T. Friend ments on the submitted paper.

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