The Madagascan Cuckoo-roller (Aves: Leptosomidae) is not a roller notes on the phylogenetic affinities and evolutionary history of a living fossil

ACTA ORNITHOLOGICA Vol. 43 (2008) No. 2 SHORT NOTES The Madagascan Cuckoo-roller (Aves: Leptosomidae) is not a roller notes on the phylogenetic affinities and evolutionary history of a living fossil Gerald MAYR Forschungsinstitut Senckenberg, Sektion Ornithologie, Senckenberganlage 25, D-60325 Frankfurt am Main, GERMANY, e-mail: Gerald.Mayr@senckenberg.de Mayr G. 2008. The Madagascan Cuckoo-roller (Aves: Leptosomidae) is not a roller notes on the phylogenetic affinities and evolutionary history of a living fossil. Acta Ornithol. 43: 226 230. DOI 10.3161/000164508X395360 Abstract. The phylogenetic affinities and evolutionary history of the Madagascan Leptosomidae (Courol or Cuckoo-roller ) are reviewed to rectify erroneous accounts in the recent literature. These birds are not closely related to rollers, and multiple molecular and morphological data sets congruently support their position outside the clade including Coraciiformes sensu stricto (rollers and ground rollers), Piciformes (woodpeckers and allies), and Alcediniformes (kingfishers and allies). The recent discovery that Plesiocathartes, from the Eocene of Europe and North America, is a stem lineage representative of the Leptosomidae further shows that Pan-Leptosomidae were widely distributed across the Northern Hemisphere in the early Paleogene. The Courol is among the few avian taxa which qualify as living fossils, and its persistence on Madagascar may have been facilitated by the absence of ecological factors that led to extinction of Pan-Leptosomidae elsewhere. Key words: Leptosomidae, phylogeny, fossil record, Plesiocathartes Received Oct. 2007, accepted Febr. 2008 The Courol or Cuckoo-roller, Leptosomus discolor, occurs on Madagascar and the Comoro islands (Goodman 2001) and is classified into a monotypic family Leptosomidae (often incorrectly spelled Leptosomatidae, which refers to a taxon of nematodes). It is a carnivorous, forest dwelling bird, which breeds in natural tree cavities and feeds mainly on chameleons, geckos, and larger insects in the upper parts of the forest canopy (Goodman 2001). The Courol is considered to be most closely related to the Coraciidae (true rollers) and Brachypteraciidae (ground rollers) in even the most recent reviews and classifications, (e.g., Good man 2001, Cracraft et al. 2004, Mickoleit 2004, Livezey & Zusi 2007). However, a clade including Leptosomidae, Coraciidae, and Brachy - pteraciidae is ill-founded. Cracraft (1971), in a study on the osteology of rollers, listed several shared skull features but noted that these do not prove the monophyletic nature of the rollers (p. 725). Later, he considered his earlier study insufficiently comparative and expressed doubts on the affinities of Leptosomus (Cracraft 1981). Maurer & Raikow (1981) mentioned two myological apomorphies supporting a clade including Leptosomidae, Coraciidae, and Brachypteraciidae. One of these was considered a weak character by the authors themselves (Maurer & Raikow 1981: 427), the other is absent in Eurystomus (Coraciidae) and unknown for Brachypteraciidae which were not examined. Burton (1983) remarked on differences in the feeding apparatus of Leptosomidae and Cora - ciidae and noted that the cuckoo-roller's regular consumption of chameleons is certainly unusual, but these would hardly seem to require different adaptations from Coracias which also feeds on lizards (p. 426). Sibley & Ahlquist (1990: Fig. 359) placed Leptosomus as the sister taxon of the rollers in the summary tree of their DNA-DNA hybridization studies, but such a position is not supported by the underlying data (Mayr 1998: 10, 2008, Harshman 2007: 9). Likewise, Cracraft et al. (2004: Fig. 27.10) considered Leptosomus to be the sister taxon of

SHORT NOTES 227 Coraciidae and Brachypteraciidae although the Courol was not included in their phylogenetic analyses. Even more surprisingly in the light of evident differences in osteology between Leptosomidae and rollers, the analysis of 2954 morphological characters by Livezey & Zusi (2007) resulted in a sister group relationship be - tween Leptosomidae and Brachypteraciidae with a bootstrap support of 100%. However, as I detailed elsewhere (Mayr 2008), there are incorrect character scorings for Leptosomus in the character matrix on which this analysis is based (Livezey & Zusi 2006), and many characters were erroneously assigned the same state as in the Brachypteraciidae. Herremans & Louette (1992) and Mayr (1998) questioned a closer relationship between Lepto - somidae and rollers. For the first time Leptosomus was subjected to a cladistic analysis including all other higher land birds by Mayr et al. (2003), who also performed the first cladistic analysis including gene sequences of this taxon. Although these and subsequent analyses of the modified morphological character matrix by Mayr (2005) and Manegold (2005) failed to yield a congruent outcome concerning the sister taxon of the courol, none of them supported a closer relationship to the Coraciiformes sensu stricto (Brachy pteraciidae and Coraciidae). The latter were shown to be within a clade including Piciformes (woodpeckers and allies) and Alcediniformes (kingfishers, beeeaters, and allies). Recent Bayesian analyses of two independent molecular data sets by Ericson et al. (2006) also retained a clade including Coraciiformes sensu stricto, Piciformes, and Alcediniformes, but excluding Leptosomus (Fig. 1). MORPHOLOGICAL EVIDENCE The Coraciiformes sensu stricto, Piciformes, and Alcediniformes share the following derived morphological characters which are absent in the Leptosomidae and most other birds (Mayr 2008): 1) the mandible of the hatchling projects distinctly beyond the upper beak (Manegold 2005), 2) the proximal section of the medial margin of the tarsometatarsus forms a sharp ridge (Mayr et al. 2003), and 3) the greater ventral coverts of the secondaries are reduced (Manegold 2005). The nestlings of Piciformes, Coraciiformes sensu stricto, and Alcediniformes further share the derived lack of neoptile feathers, whereas those of Leptosomus are covered with long, white down (Good - man 2001: 394). Leptosomidae have no fossil record on Mada - gascar (Hawkins & Goodman 2003). However, several putative stem lineage representatives were described from Northern Hemispheric Fig. 1. Position of Leptosomidae in two gene trees resulting from Bayesian analyses of Ericson et al. (2006). (A) Combined sequences of c-myc (exon 3), RAG-1, myoglobin (intron 2), and ornithine decarboxylase (introns 6 and 7 with intercepting exon 7) (after Ericson et al. 2006: fig. ESM-6). (B) β-fibrinogen (intron 7) (after Ericson et al. 2006: fig. ESM-4). Nodes which received a posterior probability below 50% are collapsed, posterior probabilities of 95% or more are indicated next to the nodes. Leptosomidae and the clade including Piciformes, Alcediniformes, and Coraciiformes sensu stricto are highlighted.

228 SHORT NOTES deposits in recent years. All of these were classified into the taxon Plesiocathartes Gaillard, 1908 which comprises five species from the Lower and Middle Eocene of Europe and North America (Mourer-Chauviré 2002, 2006, Mayr 2002a, b, Weidig 2006). Especially the very well preserved holotype of Plesiocathartes major from the North American Green River Formation permits detailed osteological comparisons with L. discolor that were not possible at the time the first skeletons of Plesiocathartes were described (Mayr 2002a, b). The bones of this specimen are for the first time figured in detail and directly compared with those of extant L. discolor in the present note (Fig. 2). The P. major holotype is of particular interest because it exhibits a well-preserved coracoid, which was unknown at the time the taxon was first hypothesized to be a stem lineage representative of the Leptosomidae (Mayr 2002a, b). As already noted by Weidig (2006), the bone closely resembles the characteristic coracoid of Leptosomus (Fig. 2), and thus provides further evidence for the hypothesis that Plesiocathartes is a stem lineage representative of the Leptosomidae. Most notably, it exhibits a foramen nervi supracoracoidei and a cup-like cotyla scapularis, presumably plesiomorphic features which are absent in Coraciiformes sensu stricto, Piciformes, Alcediniformes, and most other taxa of the higher land bird assemblage (sensu Mayr et al. 2003). As detailed by Mayr (2002a, b), Plesiocathartes further shares with the extant Courol a derived morphology of the tibiotarsus (condyli very low and widely separated) and tarsometatarsus (hypotarsus with two furrows which are closed to canals in Leptosomus, trochlea metatarsi II reaching farther distally than trochlea metatarsi IV). CONCLUSIONS From the evidence outlined above, it can be concluded that the Courol is not closely related to rollers and that fossil representatives of Fig. 2. Left coracoid (dorsal view; A, B), furcula (C, D), proximal end of left humerus (caudal view; E, F), sternum (dorsolateral view; G, H), and tarsometatarsus (I, J: right one in dorsolateral [I] and dorsal [J] view; K, L: left one in plantar view) of Plesiocathartes major (holotype; Wyoming Dinosaur Center, Thermopolis, USA, WDC-2001-CGR-022) (A, C, E, G, I, K) and Leptosomus discolor (B, D, F, H, J, L) in comparison. Fossil specimens coated with ammonium chloride. Abbreviations: fns foramen nervi supracoracoidei, ila incisura lateralis, ime incisura medialis, lco left coracoid, lsc left scapula. Scale bars equal 5 mm.

SHORT NOTES 229 Pan-Leptosomidae (i.e., the total group including stem and crown group representatives) had a wide distribution over the Northern Hemisphere in the Eocene. Leptosomidae are the only avian taxon which has been recorded from the Paleogene of the Northern Hemisphere and whose crown group representatives occur exclusively on Madagascar. Clearly, stem group Leptosomidae reached Mada - gascar by dispersal, as this island separated from India in the Cretaceous and was isolated from other land masses since that time (e.g., Smith et al. 1994). All dated specimens of fossil Lepto somidae come from Eocene deposits, and these birds may thus have already disappeared from the Northern Hemisphere towards the Oligocene. However, when the ancestors of extant Lepto so midae dispersed onto the island is un known, and likewise it cannot be said whether they came from continental Africa, as apparently did the ancestors of the extant mammalian clades found on Madagascar (Poux et al. 2005), or from Southern Asia, as has been assumed for several avian taxa (e.g., Dorst 1972). Despite an intervening time span of about 50 million years, the Courol is remarkably similar to the Palaeogene stem group representatives in os - te ology (Fig. 2, Mayr 2002a, b, Weidig 2006). It could thus well qualify as a living fossil, and fulfills the criteria listed by Thenius (2000: 18) to de - fine the latter, i.e., an isolated systematic position and relict distribution, classification into a group with only few extant species, and presence of few morphological changes compared to fossil stem lineage representatives. Its persistence on Mada - gascar may have been facilitated by the absence of ecological factors, which led to the extinction of stem lineage representatives on the Northern Hem i sphere and anywhere else outside the island. ACKNOWLEDGEMENTS I thank S. Tränkner for taking the photographs, and A. Elżanowski and an anonymous referee for comments which improved the manuscript. REFERENCES Burton P. J. K. 1983. Anatomy and evolution of the feeding apparatus in the avian orders Coraciiformes and Piciformes. Bulletin of the British Museum (Natural History), Zoology series 47: 331 443. Cracraft J. 1971. The relationships and evolution of the rollers: families Coraciidae, Brachypteraciidae, and Leptosomidae. Auk 88: 723 752. Cracraft J. 1981. Toward a phylogenetic classification of the recent birds of the world (Class Aves). Auk 98: 681 714. Cracraft J., Barker F. K., Braun M., Harshman J., Dyke G. J., Feinstein J., Stanley S., Cibois A., Schikler P., Beresford P., García-Moreno J., Sorenson M. D., Yuri T., Mindell D. P. 2004. Phylogenetic relationships among modern birds (Neornithes): toward an avian tree of life. In: Cracraft J., Donoghue M. (eds). Assembling the Tree of Life. Oxford Univ. Press, New York. pp: 468 489. Dorst J. 1972. The evolution and affinities of the birds of Madagascar. In: Battistini R., Richard-Vindard G. (eds). Biogeography and Ecology in Madagascar. W. Junk, Den Haag. pp: 615 627. Ericson P. G. P., Anderson C. L., Britton T., Elżanowski A., Johansson U. S., Källersjö M., Ohlson J. I., Parsons T. J., Zuccon D., Mayr G. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. Biol. Letters 2: 543 547. Goodman S. M. 2001. Family Leptosomidae (Cuckoo-rollers). In: del Hoyo J., Elliott A., Sargatal J. (eds). Handbook of the Birds of the World. Vol. VI. Mousebirds to Hornbills. Lynx Edicions, Barcelona. pp: 390 395. Harshman J. 2007. Classification and Phylogeny of Birds. In: Jamieson B. G. M. (ed.). Reproductive Biology and Phylogeny of Birds. Science Publishers, Enfield (NH). pp: 1 35. Hawkins A. F. A., Goodman S. M. 2003. Introduction to the Birds. In: Goodman S. M., Benstead J. P. (eds). The Natural History of Madagascar. Univ. Chicago Press, Chicago. pp: 1019 1044. Herremans M., Louette M. 1992. Sexual dimorphism in the juvenile plumage of the Courol Leptosomus discolor and considerations on its affinities. Bull. British Ornithol. Club 112: 182 185. Livezey B. C., Zusi R. L. 2006. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy: I. Methods and characters. Bull. Carnegie Mus. Nat. Hist. 37: 1 544. Livezey B. C., Zusi R. L. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. II. Analysis and discussion. Zool. J. Lin. Soc. 149: 1 95. Manegold A. 2005. Zur Phylogenie und Evolution der Racken -, Specht- und Sperlingsvögel ( Coraciiformes, Piciformes und Passeriformes: Aves). dissertation.de, Berlin. Maurer D., Raikow R. J. 1981. Appendicular myology, phylogeny, and classification of the avian order Coraciiformes (including Trogoniformes). Ann. Carnegie Mus. Nat. Hist. 50: 417 434. Mayr G. 1998. Coraciiforme und piciforme Kleinvögel aus dem Mittel-Eozän der Grube Messel (Hessen, Deutsch - land). Courier Forschungsinstitut Senckenberg 205: 1 101. Mayr G. 2002a. Avian Remains from the Middle Eocene of the Geiseltal (Sachsen-Anhalt, Germany). In: Zhou Z., Zhang F. (eds). Proc. 5 th Symposium Soc. Avian Paleontol. Evol., Beijing, 1 4 June 2000. Science Press, Beijing. pp: 77 96. Mayr G. 2002b. A new species of Plesiocathartes (Aves: Lepto - somidae) from the Middle Eocene of Messel, Germany. PaleoBios 22: 10 20. Mayr G. 2005. A Fluvioviridavis-like bird from the Middle Eocene of Messel, Germany. Can. J. Earth Sci. 42: 2021 2037. Mayr G. 2008. Avian higher-level phylogeny: well-supported clades and what we can learn from an analysis of 2954 morphological characters. J. Zool. Syst. Evol. Res. 46: 63 72.

230 SHORT NOTES Mayr G., Manegold A., Johansson U. 2003. Monophyletic groups within higher land birds comparison of morphological and molecular data. J. Zool. Syst. Evol. Res. 41: 233 248. Mickoleit G. 2004. Phylogenetische Systematik der Wirbeltiere. Friedrich Pfeil, München. Mourer-Chauviré C. 2002. Revision of the Cathartidae (Aves, Ciconiiformes) from the Middle Eocene to the Upper Oligocene Phosphorites du Quercy, France. In: Zhou Z., Zhang F. (eds). Proc. 5 th Symposium Soc. Avian Paleontol. Evol., Beijing, 1 4 June 2000. Science Press, Beijing. pp: 97 111. Mourer-Chauviré C. 2006. The avifauna of the Eocene and Oligocene Phosphorites du Quercy (France): an updated list. Strata, série 1, 13: 135 149. Poux C., Madsen O., Marquard E., Vieites D. R., de Jong W. W., Vences M. 2005. Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Syst. Biol. 54: 719 730. Sibley C. G., Ahlquist J. E. 1990. Phylogeny and classification of birds: A study in molecular evolution. Yale Univ. Press, New Haven. Smith A. G., Smith D. G., Funnell B. M. 1994. Atlas of Mesozoic and Cenozoic coastlines. Cambridge Univ. Press, Cambridge. Thenius E. 2000. Lebende Fossilien: Oldtimer der Pflanzenund Tierwelt. Friedrich Pfeil, München. Weidig I. 2006. The first New World occurrence of the Eocene bird Plesiocathartes (Aves: Leptosomidae). Paläonto lo gische Zeitschrift 80: 230 237. STRESZCZENIE [Kurol] W odpowiedzi na błędne ujęcia powtarzane w literaturze, praca ta zawiera rewizję filogenetycznych pokrewieństw i ewolucyjnej historii madagaskarskich kuroli Leptosomidae. Liczne molekularne and morfologiczne dane zgodnie wskazują, że ptaki te nie tylko nie są blisko spokrewnione z kraskami, ale nawet nie należą do kladu obejmującego kraskowe Coraciiformes sensu stricto (kraski i ziemnokraski), dzięciołowe Piciformes i zimorodkowe Alcediniformes. Co więcej, ostatnie odkrycie, że Plesiocathartes Gaillard, 1908 z eocenu Europy i Ameryki Płn. reprezentuje pienne Leptosomidae wykazuje, że Pan-Leptosomidae były szeroko rozpowszechnione we wczesnym paleogenie Półkuli Północnej. Kurol jest jednym z nielicznych ptasich taksonów, które kwalifikują się jako żyjące skamieniałości, a jego przetrwanie na Madagaskarze jest za pew - ne wynikiem braku ekologicznych czynników, które doprowadziły do wymarcia Pan-Lepto so - midae na pozostałych obszarach. T. Cofta