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Ing.Org Published in Great Britain by the Royal Society, 6–9 Carlton House Terrace, London SW1Y 5AG Coturnix Coturnix Japonica Number 1665 Number RSPB_276_1665_Cover.qxp 4/23/09 4:39 PM Page 1 Proc. R. Soc. B | vol. 276 no. 1665 pp. 2133–2331 22 June 2009 ISSN 0962-8452 volume 276 22 June 2009 number 1665 volume 276 . number 1665 . pages 2133–2331 pages 2133–2331 Review articles Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression 2133 S. Puthiyaveetil & J. F. Allen Research articles Going to great lengths: selection for long corolla tubes in an extremely specialized bat–flower mutualism 2147 N. Muchhala & J. D. Thomson Dynamics of crowing development in the domestic Japanese quail (Coturnix coturnix japonica) 2153 S. Derégnaucourt, S. Saar & M. Gahr Emperor penguin mates: keeping together in the crowd 2163 A. Ancel, M. Beaulieu, Y. Le Maho & C. Gilbert A quantum probability explanation for violations of ‘rational’ decision theory 2171 E. M. Pothos & J. R. Busemeyer Spectacular morphological novelty in a miniature cyprinid fish, Danionella dracula n. sp. 2179 R. Britz, K. W. Conway & L. Rüber Does colour polymorphism enhance survival of prey populations? 2187 L. Wennersten & A. Forsman Genetic linkage map of the guppy, Poecilia reticulata, and quantitative trait loci analysis of male size and colour variation 2195 N. Tripathi, M. Hoffmann, E.-M. Willing, C. Lanz, D. Weigel & C. Dreyer Biodiversity and body size are linked across metazoans 2209 C. R. McClain & A. G. Boyer The evolution of covert, silent infection as a parasite strategy 2217 I. Sorrell, A. White, A. B. Pedersen, R. S. Hails & M. Boots Avian orientation: the pulse effect is mediated by the magnetite receptors in the upper beak 2227 W. Wiltschko, U. Munro, H. Ford & R. Wiltschko An experimental test of the independent action hypothesis in virus–insect pathosystems 2233 M. P. Zwart, L. Hemerik, J. S. Cory, J. A. G. M. de Visser, F. J. J. A. Bianchi, M. M. Van Oers, J. M. Vlak, R. F. Hoekstra & W. Van der Werf Botanical ratchets 2243 I. M. Kulic´, M. Mani, H. Mohrbach, R. Thaokar & L. Mahadevan Why do winners keep winning? Androgen mediation of winner but not loser effects in cichlid fish 2249 R. F. Oliveira, A. Silva & A. V. M. Canário Bystanders affect the outcome of mother–infant interactions in rhesus macaques 2257 S. Semple, M. S. Gerald & D. N. Suggs Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants 2263 H. Fernández-Marín, J. K. Zimmerman, D. R. Nash, J. J. Boomsma & W. T. Wcislo What can genetic variation tell us about the evolution of senescence? 2271 J. A. Moorad & D. E. L. Promislow Intraspecific variation in testis asymmetry in birds: evidence for naturally occurring compensation 2279 S. Calhim & T. R. Birkhead Extra-pair young in house wren broods are more likely to be male than female 2285 L. S. Johnson, C. F. Thompson, S. K. Sakaluk, M. Neuhäuser, B. G. P. Johnson, S. S. Soukup, S. J. Forsythe & B. S. Masters Post-weaning maternal effects and the evolution of female dominance in the spotted hyena 2291 H. E. Watts, J. B. Tanner, B. L. Lundrigan & K. E. Holekamp Does horizontal transmission invalidate cultural phylogenies? 2299 S. J. Greenhill, T. E. Currie & R. D. Gray Cellular and humoral immunodepression in vultures feeding upon medicated livestock carrion 2307 J. A. Lemus & G. Blanco Trill consistency is an age-related assessment signal in banded wrens 2315 S. R. de Kort, E. R. B. Eldermire, S. Valderrama, C. A. Botero & S. L. Vehrencamp Temperature has a causal effect on avian timing of reproduction 2323 M. E. Visser, L. J. M. Holleman & S. P. Caro Founded in 1660, the Royal Society is the independent scientific academy of the UK, dedicated to promoting excellence in science rspb.royalsocietypublishing.org Registered Charity No 207043 Published in Great Britain by the Royal Society, 22 June 2009 6–9 Carlton House Terrace, London SW1Y 5AG Downloaded from rspb.royalsocietypublishing.org on 11 March 2009 Proc. R. Soc. B doi:10.1098/rspb.2009.0141 Published online Spectacular morphological novelty in a miniature cyprinid fish, Danionella dracula n. sp. Ralf Britz1,*, Kevin W. Conway2 and Lukas Ru¨ ber1 1Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK 2Department of Biology, Saint Louis University, 3507 Laclede Avenue, St Louis, MO 63103-2010, USA Danionella dracula is a new species of sexually dimorphic, miniature and highly developmentally truncated cyprinid fish. Compared with its close relative, the zebrafish Danio rerio, it lacks 44 bones or parts thereof and represents one of the most developmentally truncated vertebrates. Absence of the majority of bones appears to be due to developmental truncation via terminal deletion. In contrast to these larval-like features, D. dracula also shows several hyperossifications. Uniquely, among carp-like fishes, male D. dracula have a series of long, pointed odontoid processes on the jaws greatly resembling the jaw dentition of teleosts with true teeth. The anterior-most process in each jaw is extended as a canine-like fang projecting through the epithelium. True jaw teeth are absent from all 3700 species of cypriniforms and were lost at least in the Upper Eocene. It remains to be investigated, however, whether the conserved pathways to regulate tooth development in cypriniforms have been used in D. dracula to form and pattern the odontoid processes. This new species represents a remarkable example linking progenetic paedomorphosis via heterochronic change in developmental timing to the evolution of morphological novelties. Keywords: Danionella; Cypriniformes; jaw teeth; miniaturization; developmental truncation; evolutionary novelty 1. INTRODUCTION syngnathoids among teleosts. The zebrafish, a member Miniaturization, the evolution of extremely small body of the cypriniforms, has become an important model size, has been linked to the appearance of morphological organism for the study of the developmental genetic novelties (Hanken 1993; Hanken & Wake 1993). In pathways that initiate tooth formation, and recent studies vertebrates, this relationship is best documented for have demonstrated that essential parts of this pathway amphibians and fishes, the most intriguing recent example have been retained in the oral cavity during cypriniform being the cypriniform genus Paedocypris (Kottelat evolution (Jackman & Stock 2006; Stock et al. 2006; Stock et al. 2006; Britz & Conway 2009). Among cypriniforms 2007). The newly discovered species D. dracula is (carp-like fishes), the most unusual morphological novel- morphologically closer to an oral dentition than any ties are found in miniatures showing a high degree other cypriniform, but with the evolutionary acquisition of developmental truncation (Ru¨ber et al. 2007; Britz & of its odontoid processes, it has clearly followed an Conway 2009). Here, we report the discovery of a new alternative route to the re-evolution of jaw teeth. The miniature species of cypriniform, Danionella dracula n. sp., present paper describes this unique cypriniform fish, its which is closely related to the zebrafish (Danio rerio) and, unusual jaw anatomy and developmentally truncated even when adult, shows a remarkably larval-like skeleton. skeleton, and highlights its potential for addressing more This developmental truncation is associated in this species general questions about the evolutionary role of hetero- with the evolution of astonishing novel morphological chrony to generate morphological diversity and the characters, all of them sexually dimorphic. The most re-evolution of lost structures. extraordinary novelty of males of the new species is a series of odontoid processes in both the upper and lower jaws, some of which project through the epithelium as 2. MATERIAL AND METHODS true teeth. (a) Anatomical study Jaw teeth are a defining character of gnathostomes and All sizes are of a standard length (SL; from tip of the lower jaw are almost universally present in various shapes and sizes to the end of hypural complex in millimetres). Measurements ! among the 50 000 species of jawed vertebrates. Jaw teeth were made at 10 magnification using a stereomicroscope have been lost repeatedly during the evolution of equipped with an ocular micrometer. For the study of gnathostomes, with turtles and birds being the most the skeleton, 10 males and 10 females were cleared and prominent examples. Among bony fishes, teeth are also double stained for bone and cartilage (Taylor & Van Dyke absent from the jaws of all gonorynchiforms and cyprini- 1985). For the histological study of the odontoid processes, forms, curimatid characiforms, and the majority of a 16.7 mm male was embedded in paraplast, serially sectioned at 8 mm, and the sections were stained with Azan- Domagk. Specimens and sections were photographed with a * Author for correspondence ([email protected]). Jenoptik ProgRes 12 C digital camera on a Zeiss Tessovar or Electronic supplementary material is available at http://dx.doi.org/10. a Zeiss Axiocam HRc on a Zeiss Discovery V20. One male 1098/rspb.2009.0141 or via http://rspb.royalsocietypublishing.org. was prepared for scanning electron microscopy; it was Received 26 January 2009 Accepted 13 February 2009 1 This journal is q 2009 The Royal Society Downloaded from rspb.royalsocietypublishing.org on 11 March 2009 2 R. Britz et al. Morphological novelty in a cyprinid fish critical-point dried and sputter coated with palladium– sampling for 3 000 000 generations (two independent runs gold and observed and photographed in a Philips Xl-30 each with four simultaneous MC chains; chain temperature FEG SEM. All specimens are deposited in the Natural 0.2; sample frequency 300 under the GTRCICG model as History Museum (BMNH), London. selected by MODELTEST v. 3.7). The cytb dataset was run with seven data partitions (first, second and third codon positions (b) Biological material, DNA isolation, PCR for the combined mitochondrial protein-coding genes (cytb and DNA sequencing and cox1) and the nuclear RAG1, respectively, and the To assess the phylogenetic position of D.
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