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Repeated Evolution of Fused Thoracic Vertebrae in Songbirds

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Repeated Evolution of Fused Thoracic Vertebrae in Songbirds The Auk 126(4):862−872, 2009 The American Ornithologists’ Union, 2009. Printed in USA. REPEATED EVOLUTION OF FUSED THORACIC VERTEBRAE IN SONGBIRDS HELEN F. JAMES 1 Department of Vertebrate Zoology, MRC-116, National Museum of Natural History, Smithsonian Institution, P.O. Box 37012, Washington, D.C. 20013, USA Abstract.—The fusion of two or more thoracic vertebrae, independent of the synsacrum, is more widespread in the Passeriformes than has previously been reported. The bone thus formed is known as a “notarium.” I surveyed oscine passerine skeletons and found a notarium with fully fused vertebrae in Chabert’s Vanga (Leptopterus chabert), certain woodswallows (Artamidae) and shrikes (Laniidae), the Willie Wagtail (Rhipiduridae, Rhipidura leucophrys), the Phainopepla (Bombycillidae, Phainopepla nitens), the penduline tits (Remizidae) including the Verdin (Auriparus flaviceps), various larks (Alaudidae), the Common Starling (Sturnus vulgaris), the sickle- billed thrashers (Toxostoma spp.), and the crossbills (Loxia spp.). Mapping of character evolution on a supertree suggests that a fully fused notarium has evolved independently at least 12 times in the oscine passerines and that notaria with less extensive fusion of the vertebrae (only the spinous processes fused, for example) are even more widespread phylogenetically. Phenotypic expression of a notarium is fixed in some species and higher taxonomic groups but varies within the species in others. Ontogenetically, the fully fused notarium forms when the bird is immature. The evolutionary development of notaria probably depends on mutations that alter expression patterns of transcription genes (Pax and Hox genes are likely candidates) that control embryological differentiation of the vertebrae. Among the systematic implications of this study are additional support for placement of the Verdin in the Remizidae and for the monophyly of a group of western thrashers (Toxostoma spp.) with strongly decurved bills. Received 2 October 2008, accepted 3 May 2009. Key words: convergent evolution, notarium, oscine, osteology, Passeri, synsacrum. Evolución Repetida de Vértebras Torácicas Fusionadas en Aves Canoras Resumen.—La fusión de dos o más vértebras torácicas, independientemente del sinsacro, es un fenómeno que está más ampliamente distribuido entre los paseriformes que lo que se había documentado previamente. El hueso que se forma de este modo se llama notario. Hice una evaluación de esqueletos de aves paserinas y observé la presencia de un notario con vértebras completamente fusionadas en Leptopterus chabert, algunos Artamidae y Laniidae, Rhipidura leucophrys, Phainopepla nitens, los Remizidae incluyendo a Auriparus flaviceps, varios Alaudidae, Sturnus vulgaris y las especies de los géneros Toxostoma y Loxia. El mapeo de la evolución de este rasgo sobre un superárbol sugiere que un notario completamente fusionado ha evolucionado independientemente al menos 12 veces en los paseriformes oscinos y que notarios con fusión menos completa de las vértebras (por ejemplo, con sólo los procesos espinosos fusionados) están aún más ampliamente distribuidos filogenéticamente. La expresión fenotípica de un notario está fija en algunas especies y grupos taxonómicos mayores, pero varía entre individuos en otras especies. Ontogenéticamente, el notario completamente fusionado se forma cuando el ave es inmadura. El desarrollo evolutivo de los notarios probablemente depende de mutaciones que alteran los patrones de expresión de genes de transición (los genes Pax y Hox son candidatos probables) que controlan la diferenciación embriológica de las vértebras. Entre las implicaciones sistemáticas de este estudio se encuentran el apoyo adicional para la ubicación de Auriparus en la familia Remizidae y para la monofilia de un grupo de mímidos occidentales Toxostoma( spp.) con picos fuertemente decurvados. All birds dating back at least to Archaeopteryx have a series of notaria principally involve fusion of thoracic vertebrae, the def- vertebrae adjacent to the ilium that are fused together, forming a inition should be amended to include the caudal-most cervical bone called the “synsacrum”; all modern birds also have several vertebra, which sometimes participates. Notaria occur in an eco- fused terminal caudal vertebrae that form the pygostyle. Some logically disparate assortment of nonpasserine birds, including birds have a third series of fused vertebrae, the notarium, defined ground-dwelling birds (e.g., Galliformes, Tinamiformes, Columbi- as any group of thoracic vertebrae that are fused to each other formes, and various Gruiformes), waders (e.g., Threskiornithidae, but not to the synsacrum (Baumel and Witmer 1993). Although Phoenicopteridae, and Gruidae), divers (e.g., Podicipediformes 1E-mail: [email protected] The Auk, Vol. 126, Number 4, pages 862−872. ISSN 0004-8038, electronic ISSN 1938-4254. 2009 by The American Ornithologists’ Union. All rights reserved. Please direct all requests for permission to photocopy or reproduce article content through the University of California Press’s Rights and Permissions website, http://www.ucpressjournals. com/reprintInfo.asp. DOI: 10.1525/auk.2009.08194 — 862 — 14_James_08-194.indd 862 9/2/09 2:46:39 PM OCT O BER 2009 — FUSED VERTEBRAE IN SO NGBIRDS — 863 and some Phalacrocoracidae), certain arboreal types (Steatornis, Sturnidae on the basis of a more recent, comprehensive paper for Opisthocomus, and Forpus), and in the falcons (Falconidae). Fused that clade (Lovette and Rubenstein 2007). vertebrae are of interest because they are a clearly definable osteo- Based on the supertree, a phylogenetic tree covering as many logical trait, useful in systematics, for the identification of fossils, of the taxa examined as possible was constructed using MAC- and for studies of patterns in evolution of the avian skeleton. CLADE, version 4.08 (Maddison and Maddison 2005). In cases Three previous surveys of the distribution of notaria in birds in which the genus but not the species examined was present in gave scant attention to the Passeriformes. Rydzewski (1935) re- the supertree, I substituted the species I examined or added it in ported finding fused vertebrae in three species of larks; Storer a polytomy with other members of the genus. This was not done (1982) found the trait to be absent in his family-level survey of if there was ambiguity about where to add the species. Ambigu- the Passeriformes; and Samejima and Otsuka (1984) found it ity would occur if the genus was depicted as polyphyletic in the present only in a species of weaver finch. Being familiar with supertree or if there was a resolved branching pattern within the Storer’s paper, I was surprised to find a fully fused notarium genus that would need to be collapsed in order to add the species involving three to four thoracic vertebrae in the penduline tits in a polytomy. (Remizidae), including the Verdin (Auriparus flaviceps). I incor- My observations of patterns of fusion were coded as a simple porated my observations in the data matrix for a previous paper character with three states. Instances of intraspecific polymor- without further elaboration (James et al. 2003: character 41). The phism were recorded as multistate taxa; the few cases in which the discovery inspired me to undertake a more thorough survey of state could not be determined were coded as “uncertainty.” Charac- oscine skeletons, with the aim of documenting the distribution ter-state changes were then mapped on the phylogeny using MES- of notaria and laying the foundation for study of their evolution- QUITE (see Acknowledgments), with the parsimony criterion. ary history. RESULTS METHODS For reference, Figure 1K shows the vertebral column and articulat- I examined >500 skeletons of oscine passerines, most of them in ing postcranial bones of the Black-capped Chickadee (Poecile atri- the collection of the National Museum of Natural History (USNM, capillus), a species that lacks a notarium. As is typical of passerine Washington, D.C.). The taxonomic sample included ~250 genera birds, there are five free thoracic (also called “dorsal”) vertebrae, all and ~350 species, encompassing 80% of the 82 oscine families rec- of which connect to the sternum via a vertebral and a sternal rib. ognized by Dickinson (2003). For each species, I examined one or The last cervical vertebra has a floating vertebral rib attached to it, a few adult skeletons, and if fused vertebrae were found, I then ex- with no corresponding sternal rib. The sixth complete pair of ribs amined a broader sample of that species (including immatures) and in the sequence articulates with the first vertebra in the synsacrum related species, provided that skeletons were available. I recorded dorsally and with the fifth sternal rib (rather than directly with the whether the braincase was double-walled (pneumatic) as in adult sternum) ventrally; thus, it is not associated with a thoracic verte- birds or partly single-walled as in immatures and described any bra. There are three places where the vertebrae contact each other fusion of thoracic (and caudal cervical) vertebrae. Vertebral col- and, therefore, can potentially fuse: the articular surfaces of the cor- umns of smaller birds were examined under 6−50× magnification pus vertebrae (vertebral bodies), the articular surfaces of the zyga- using a dissecting microscope. Birds that died in captivity were pophyses, and the expansive spinous processes that project dorsad excluded from the sample except where noted. Dickinson (2003) and help
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