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Spatangoid Echinoids During the Late Cretaceous Coordinated Shifts To Downloaded from rsbl.royalsocietypublishing.org on 11 September 2009 Coordinated shifts to non-planktotrophic development in spatangoid echinoids during the Late Cretaceous John A. Cunningham and Charlotte H. Jeffery Abt Biol. Lett. 2009 5, 647-650 first published online 10 June 2009 doi: 10.1098/rsbl.2009.0302 Supplementary data "Data Supplement" http://rsbl.royalsocietypublishing.org/content/suppl/2009/06/08/rsbl.2009.0302.DC1.ht ml References This article cites 21 articles, 12 of which can be accessed free http://rsbl.royalsocietypublishing.org/content/5/5/647.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections evolution (1019 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Biol. Lett. go to: http://rsbl.royalsocietypublishing.org/subscriptions This journal is © 2009 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on 11 September 2009 Biol. Lett. (2009) 5, 647–650 development to non-planktotrophic development. doi:10.1098/rsbl.2009.0302 This has been inferred by mapping larval modes onto Published online 10 June 2009 phylogenetic trees of various taxa (e.g. echinoids Palaeontology (Wray 1992; Smith et al. 1995); temnopleurid echinoids (Jeffery & Emlet 2003; Jeffery et al. 2003); asterinid starfish (Hart et al. 1997); Conus gastropods Coordinated shifts to (Duda & Palumbi 1999); littorinid gastropods (Reid 1989); turritellid gastropods (Lieberman et al. non-planktotrophic 1993)). We now know a great deal about the develop- mental and genetic changes involved in these switches development in spatangoid owing, in particular, to the large body of work on the echinoids during the Late non-planktotrophic echinoid Heliocidaris erythro- gramma and the closely related Heliocidaris tuberculata, Cretaceous which has planktotrophic development (reviewed by Raff & Byrne 2006). However, an important, and yet John A. Cunningham* and Charlotte H. Jeffery Abt much overlooked, issue is when these switches to Department of Earth and Ocean Sciences, University of Liverpool, non-planktotrophy occurred: were shifts to non- 4 Brownlow Street, Liverpool L69 3GP, UK planktotrophy scattered randomly through time, or *Author and address for correspondence: Department of Earth Sciences, were they instead concentrated in particular intervals University of Bristol, Wills Memorial Building, Queen’s Road, Bristol BS8 1RJ, UK ( [email protected]). of geological history? The question is important as it may help to determine the factors that drive shifts to Despite widespread interest in the interplay non-planktotrophy. If the switches were concentrated between evolutionary and developmental pro- in particular time intervals, then this would strongly cesses, we still know relatively little about the evolutionary history of larval development. imply that extrinsic factors operating at these Many clades exhibit multiple shifts from times are responsible for driving the switches to planktotrophic (feeding) to non-planktotrophic non-planktotrophy. (non-feeding) larval development. An important The tacit assumption among biologists appears to question is whether these switches are scattered be that the switches were scattered randomly through- randomly through geological history or are con- out geological history (Jeffery 1997). However, when centrated in particular intervals of time. This Jeffery (1997) carried out a broad survey of all major issue is addressed using the Cretaceous spatan- echinoid clades, she found that the first known occur- goid sea urchins, which are unusual in that rence of non-planktotrophy in five different orders lay larval strategy can be determined unambiguously in the final two stages of the Cretaceous (the Campa- from abundantly fossilized adult tests. Using a genus-level phylogeny, we identify five clades of nian and Maastrichtian), with no examples of non-planktotrophic taxa, each of which first non-planktotrophic echinoids known from earlier appears in the fossil record in the Campanian than this interval. Despite this study, little is known or Maastrichtian (the final two Cretaceous about the finer scale patterns within orders and at stages). No examples of non-planktotrophy have lower taxonomic levels. The present study addresses been identified in any of the earlier stages of the this by focusing in detail on a single echinoid order, Cretaceous. This strongly suggests that shifts to the Spatangoida. non-planktotrophic development are clustered in certain episodes of geological history, and this, in turn, implies that extrinsic factors oper- 2. MATERIAL AND METHODS ating at these times are responsible for driving (a) Choice of model organism shifts in developmental strategy. The Cretaceous spatangoid echinoids were chosen as the model organism for this study as they are ideal for a number of reasons: Keywords: non-planktotrophy; planktotrophy; (i) they are unusual in that larval strategy can be inferred from the echinoids; spatangoids; Cretaceous fossilized adult test using either morphological criteria or crystallo- graphic analysis of the apical system (discussed subsequently); (ii) they are abundantly preserved, usually with the apical system pre- sent, providing a large volume of suitable material for analysis; (iii) their complex morphology makes it relatively straightforward 1. INTRODUCTION to establish their phylogenetic relationships; and (iv) the group Most marine invertebrates employ one of two distinct contains both planktotrophic and non-planktotrophic taxa and strategies for larval development. In the first of these, spans the time when non-planktotrophy is thought to have first termed planktotrophy, the larvae feed in the water evolved within the group. column for a period of weeks or months before they (b) Inferring modes of larval development settle and metamorphose into juveniles. In the alterna- Larval modes were determined for 87 fossil spatangoid specimens tive strategy, termed non-planktotrophy, the larvae are from museum collections that span the early history of the group produced in much smaller numbers and do not feed, (see electronic supplementary material for details). Three criteria were used for inferring the mode of larval development from adult but instead are supplied with nourishment in the fossil sea urchin specimens. form of an egg yolk for the much shorter period they spend either living in the water column or being (i) Identification of brood pouches (marsupia). Some non- brooded prior to metamorphosis. planktotrophic taxa brood their larvae and a subset of these do so in specialized brood pouches on the test of the A common theme that has been identified is for female; the identification of such marsupia is indicative of clades to exhibit multiple shifts from planktotrophic non-planktotrophic development (e.g. Kier 1969). (ii) Extreme sexual dimorphism of gonopore size. Because non- Electronic supplementary material is available at http://dx.doi.org/ planktotrophic taxa have much larger eggs (Emlet et al. 10.1098/rsbl.2009.0302 or via http://rsbl.royalsocietypublishing.org. 1987; Emlet 1989), the females frequently have enlarged Received 14 April 2009 Accepted 20 May 2009 647 This journal is q 2009 The Royal Society Downloaded from rsbl.royalsocietypublishing.org on 11 September 2009 648 J. A. Cunningham & C. H. Jeffery Abt Larval mode in spatangoid echinoids Orthaster Cyclaster Stage Holanthus Isaster Abatus Mecaster Mauritanaster Mokotibaster Micraster Lambertiaster Holcopneustes Bolbaster Iraniaster Leiostomaster Hemiaster Linthia Heterolampas Leymeriaster Diplodetus Homoeaster Schizaster Tessieria Proraster Plesiaster Ovulaster Coraster Cottreaucorys Maas Gibbaster 70 Turanglaster Camp 80 Sant Periaster Con Polydesmaster 90 Tur Heteraster Pliotoxaster Macraster Cen Palhemiaster 100 Epiaster Age Alb (Ma) 110 Toxaster Apt 120 Bar 130 Haut Val 140 Ber Figure 1. Strict consensus tree of Cretaceous spatangoid genera plotted against the geological time scale. Planktotrophic taxa are shown in red, non-planktotrophic taxa in blue and unknown development in grey. Coloured circles represent specimens for which development has been inferred. The green band highlights the Campanian to Maastrichtian interval. Analysed speci- mens of Holanthus, Cyclaster and Orthaster are Danian in age (see electronic supplementary material for details of phylogenetic analysis and specimens studied). gonopores through which to extrude these eggs. Extreme sexual strategy observed prior to this. The Campanian to dimorphism can indicate non-planktotrophic development Maastrichtian is also the interval during which the (Emlet 1989), although gonopores can also be enlarged by dissolution (S. K. Donovan 2008, personal communication). first known instance of non-planktotrophy in four (iii) Crystallographic orientation of the apical plates. Larval other echinoid orders has been recorded; there are no mode can be inferred from the orientation of the crystallo- reported occurrences of non-planktotrophy in echinoids graphic axes of the plates in the apical system (Emlet 1985, 1989). This is possible because planktotrophic from any time earlier than this (Jeffery 1997). larvae have skeletal calcite rods, the main function of which is to support the larval arms that are used in feeding; during metamorphosis some of the apical plates grow from 4. DISCUSSION the proximal ends of the rods, imparting characteristic
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