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INTERGENERIC RELATIONSHIPS of the NEW WORLD JAYS INFERRED from CYTOCHROME B GENE SEQUENCES

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INTERGENERIC RELATIONSHIPS of the NEW WORLD JAYS INFERRED from CYTOCHROME B GENE SEQUENCES The Condor 99:490-502 0 The Cooper Ornithological Society 1997 INTERGENERIC RELATIONSHIPS OF THE NEW WORLD JAYS INFERRED FROM CYTOCHROME b GENE SEQUENCES ALEJANDROESPINOSA DE LOS MONTEROS AND JOEL CRACRAFT Department of Ornithology, American Museum of Natural History, Central Park West @ 79th Street, New York, NY 10024, e-mail: [email protected] Abstract. The six genera of corvids endemic to the Americas (i.e., Aphelocoma, Calo- citta, Cyanocitta, Cyanocorax, Cyanolyca, and Gymnorhinus) form the assemblagethat most ornithologistscall the New World jays. The intergenericrelationships among these six gen- era are explored using complete sequencesfrom the cytochrome b gene (1,143 bp) along with 29 morphologicalcharacters. A consistentphylogenetic hypothesis was obtained when the data sets were analyzed independently or in a total evidence approach.The phylogeny presentedin this paper does not corroboratethe existence of two evolutionary lineages as previously proposedby Hardy (1961, 1969). The most basal genus of the New World jays is Cyanolyca, which also is supportedby independent evidence on cranial anatomy. The remainder of the genera are embeddedwithin two major clades. The most derived is formed by Cyanocitta, Aphelocoma, and Gymnorhinus, being Cyanocitta the most basal genuswith- in this clade. Calocitta and Cyanocorax constitutethe otherclade. A very closerelationship betweenthese two generais supportedby bootstrapvalues and branchsupport analysis. Theseresults corroborate the hypothesisthat the Piiion Jay (Gymnorhinus cyanocephalus) is a true New World jay, and a putative relationship with nutcrackersis not supported.The phylogeny obtainedis usedto infer a biogeographicscenario, as well to explain the evolution of a very derived jaw articulationpresent only in the New World jays. The biogeographic scenario agrees with a relatively recent arrival of a corvine ancestor via Beringia, and a very rapid dispersaland radiation into the Americas. Key words: New World jays, Corvidae, cytochrome b gene, total evidence analysis, phylogenetic analysis, biogeography. INTRODUCTION ids, particularly to the genus Nucifraga, based Corvids (crows, jays and allies) are one of the on the fact that Gymnorhinus walks and runs most successful groups of passerine birds. The instead of hops as do all the New World jays. family has a world-wide distribution and exhib- Hardy argued that the walking behavior must be its a high speciesdiversity. The corvids encom- correlated with a rather different neuromuscular pass a total of 25 genera and 113 species,which control system. Other workers have acceptedthe are found in numerous kinds of habitats (Good- idea that the Pifion Jay is related to the other win 1976, Madge and Bum 1994). Six genera jays, but they have usually postulated that Gym- norhinus of corvids (i.e., Aphelocoma, Calocitta, Cyano- is basal and should be considered as the sister-group to the New World jays (Ashley citta, Cyanocorax, Cyanolyca, and Gymnorhin- us, sensu AOU 1983) are endemic to the Amer- 1941, Pitelka 1951, Goodwin 1976). icas and have successfully radiated within trop- Not only has the position of the Pifion Jay ical, subtropical, and mild temperate environ- been challenged, but the entire phylogenetic ar- ments. Some morphological characters, like a rangement of the New World jays has been con- buttress complex (Zusi 1987), shared by these stantly questioned. Earlier workers have at- taxa seem to support their monophyly, and for tempted to resolve corvid intergeneric relation- most ornithologists these six genera comprise ships based on morphological characters (e.g., the so-called New World jays. In contrast, others Ridgway 1904, Amadon 1944, Hardy 1961, have argued that Gymnorhinus (the Pifion Jay) 1969). Despite this attention, the phylogenetic should be excluded from this assemblage. For conclusions of these studies show little congru- instance, Hardy (1961) postulated that the Pition ence. Moreover, the methods used to establish Jay was most closely related to Old World corv- monophyly of the New World jays in those anal- yses were weak, because they were based on poorly defined similarities and without evidence ’ ’ Received10 May 1996. Accepted12 December for polarity of the characters. 1996. Using external morphological and behavioral [4901 INTERGENERIC RELATIONSHIPS OF THE NEW WORLD JAYS 491 characters, Amadon (1944) postulated that all within the group showed highly unstable topol- New World jays formed a monophyletic group, ogies, her results supported the monophyly of and he placed them as the sister-group to Gym- the New World jays on the basis of four derived norhinus cyanocephalus(Pifion Jay). He consid- characters: (a) a very high rostra1 crest of the ered Gymnorhinus to be a specialized jay that lateral cotyla of the mandible, (b) a rostral artic- resembles nutcrackers (Nucifraga spp.) because ulation of the lower jaw, (c) the presence of a of similarities in feeding habits. Amadon’s clas- medial basal ridge on the quadrate, and (d) an sification divided the New World jays into four extensive fusion of the prepalatine bar to the genera, instead of the nine previously proposed ventral bar of the jaw. Hope (1989) presented by Ridgway (1904). The genera recognized by three different phylogenetic hypotheses for re- Amadon were: Cyanocitta (which included lationships within the New World jays. In all of Aphelocoma, Cyanolyca and Cissilopha), Psilo- them, however, the genera Aphelocoma and rhinus, Cyanocorax, and Calocitta (Fig. la). Cyanocorux were postulated to be paraphyletic. Hardy (1961) suggested that two main evo- Another constant result was the emergence of lutionary lineages of New World jays could be Cyanolyca as the most basal taxon. A strict con- identified using both behavioral and morpholog- sensustree of the three solutions highlights the ical evidence. He distinguished an “Inornate unresolved relationships among the New World line” (tribe Aphelocomini) containing only the members of the genus Aphelocomu, and an “Or- jays (Fig. Id). nate line” (tribe Cyanocorini) which encom- The development of molecular protocols has passed five of the remaining seven genera (Cul- allowed the integration of biochemical data into ocitta, Cissilopha, Cyanocitta, Cyanocorax, and phylogenetic analysis. Sibley and Ahlquist Psilorhinus). The genus Cyanolyca was omitted (1985) employed DNA-DNA hybridization dis- from either line becausethe speciesin this genus tances to explore the phylogenetic affinities were considered to be so poorly known behav- among corvids. Their analysis included three iorally that their affinities could not be assessed genera of New World jays (Cyanocitta, Aphel- (Fig. lb). Hardy (1969) later reviewed his pre- ocoma, and Cyanocorux). Their results show the vious classification and maintained the hypoth- New World jays as a paraphyletic group inside esis of two evolutionary lineages inside the New the tribe Corvini (sensu Sibley and Ahlquist), World jays, but this time only recognized three which also includes crows, magpies, nutcrackers genera. The ornate lineage consisted of Cyano- and coughs. It should be noted, however, that cittu, as well as the largely Neotropical Cyano- the resolving power of DNA hybridization data, corax within which Calocitta, Cissilopha, and as well as the methodology used to analyze Psilorhinus were ranked as subgenera. The in- them, have been questioned (Cracraft 1987, ornate lineage contained the third genus, Aphel- Houde 1987, Harshman 1994). ocoma, which also included the speciesformerly Several other molecular studies have ad- placed in Cyanolyca. A major problem with both dressedthe phylogenetic relationships within the of Hardy’s classification schemesis that the in- corvine assemblage (Sibley and Ahlquist 1990, ornate clade was defined mainly on the absence Helm-Bychowski and Cracraft 1993). However, of ornate plumage which seems to be a plesio- none of these studies has confronted relation- morphic condition among corvids. ships within the New World jays in detail. The Goodwin (1976) concurred with previous au- goal of the present study is to clarify the generic thors’ opinions that there was an early isolation interrelationships of these taxa by generating a of the New World jays within the corvid radia- tion. Although his classification followed Ama- new data set, namely sequencesfrom the mito- don’s hypothesis and placed the New World jays chondrial cytochrome b gene. as the sister-group of Gymnorhinus, relation- To avoid further confusion, we will use the ships within the New World jays were complete- noun “jays” when referring to the seven genera ly unresolved (Fig. lc). of corvids used in this study, and the noun Using a cladistic approach, Hope (1989) an- “New World jays” for the six genera endemic alyzed the phylogenetic interrelationships within to the Americas (Aphelocoma, Calocitta, Cya- the family Corvidae employing a set of 80 os- nocitta, Cyanocorax, Cyanolyca, and Gymno- teological characters. Although the analyses rhinus). 492 ALEJANDRO ESPINOSA DE LOS MONTEROS AND JOEL CRACRAFT (a) Amadon, 1944 (b) Hardy, 1961 Cyanocorax Cissilopha Calocitta Psilorhinus L Cyanocorax (c)Goodwin, 1976 (d) Hope, 1989 Other Corvids Other Corvids Perisoreus Corvus Cyanolyca Gymnorhinus Aphelocoma Cyanocitta Psilorhinus Cyanocorax Calocitta FIGURE 1. Some phylogenetic hypotheses previously proposed for the intergeneric relationships of New World jays. METHODS craft (1993). The Blue Jay (Cyanocittu cristutu) TAXA EXAMINED complemented the sequencesof
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