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Phylogenetic Analysis of the Cuculidae (Aves, Cuculiformes) Using Behavioral and Ecological Characters

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Phylogenetic Analysis of the Cuculidae (Aves, Cuculiformes) Using Behavioral and Ecological Characters The Auk 113(1):10-22, 1996 PHYLOGENETIC ANALYSIS OF THE CUCULIDAE (AVES, CUCULIFORMES) USING BEHAVIORAL AND ECOLOGICAL CHARACTERS JANICEM. HUGHES Departmentof Zoology,University of Toronto,Toronto, Ontario M5S 3G5, Canada AI3STRACT.--Acladistic analysis of 21 generaof cuckoos(Aves, Cuculidae)using 28 behav- ioral and ecologicalcharacters produces one shortest-lengthtree (L = 80 steps,CI = 0.52, RI = 0.79, RC = 0.42) that differs from traditional classificationsof the Cuculidae. My results suggestthat two cuculidsubfamilies, the terrestrialNeomorphinae and the Phaenicophaeinae, are polyphyletic. The obligate brood parasite Tapera(Neomorphinae) and the facultative brood parasiteCoccyzus (Phaenicophaeinae) are removedfrom otherwisenonparasitic sub- familiesand placedamong the Old World obligateparasites in the Cuculinae.This suggests that: (1) brood parasitismarose only once in the Cuculidae rather than three times as pre- viously thought; and (2) that terrestrialhabitat use in Taperahas evolved secondarily.The placementof Coccyzusamong the obligateparasites implies that the immediateancestor of this genuswas an obligatebrood parasite.Therefore, the facultativebehavior of Coccyzus representsa lossof obligateparasitism, rather than the developmentof facultativeparasitism from a nonparasiticancestor. In life, Coccyzusshares a number of life-historytraits with the obligatebrood parasites that supportthis hypothesis.Based on my analysis,I proposechanges to the classificationof the cuckoosthat are consistentwith the opinions of many early systematists,and the resultsof an unpublishedphylogeny of the cuckoosbased on postcranial osteologicalcharacters. In addition,my findingssuggest that the Hoatzin (Opisthocomushoat- zin)is a cuckoomost closely related to the communallybreeding anis (Crotophaginae). Received 12 May 1994, accepted27 January1995. THE CUCKOOSare best known for obligately ship with their hosts--that servesto minimize parasiticbreeding habits, whereby a femalewill detectionand destructionof cuckooeggs (Ham- lay eggsin the nestsof hostspecies and, hence, ilton and Orians 1965, Payne 1977, Davies and relinquish the responsibilitiesof parenthood. Brooke 1989). However, recent studies by However, this diverse family of birds, com- Brooker and Brooker (1989, 1990) have sug- prisedof 129species in 38 genera(Morony 1975), gestedthat theseadaptations to parasitismmay containsat least 4 speciesof facultative brood have evolved due to intraspecificcompetition parasites(Coccyzus spp.; Nolan and Thompson between parasiticfemales that remove an egg 1975,Ralph 1975,Sick 1993) and 74 nonparasitic from the host nest just prior to the deposition species,4 of which are communal breeders of their own egg.In addition,most cuckoo chicks (Wyllie 1981). The family is global in distri- will ejectthe host eggsor young from the nest bution and occupiesnearly all temperateand within a few days of hatching. The nestling tropicalbiomes with the exceptionof somere- Striped Cuckoo(Tapera naevia) uses mandibular mote oceanic islands. A few cuckoosare pre- hooks to kill host chicks in a manner similar to dominantly terrestrial,foraging and nestingon that of the parasitichoneyguides of the genus or near the ground; however, most speciesare Indicator(Piciformes; Morton and Farabaugh arborealand many are long-distancemigrants 1979). Theseadaptations ensure that the para- (Rowan1983). Food habits range through vary- site chick is the sole occupantof the host nest, ing degreesof herbivory and camivory with thereby improving its chancesof fledging suc- many speciesrelying almostentirely on toxic cessfully. aposomaticcaterpillars. Egg color, clutch size, The diversity of the Cuculidae may be the and incubationperiods show little consistency result of a long evolutionary history. Although throughoutthe family (Wyllie 1981).Further- the earliest known cuculid fossil dates from the more,some parasitic genera, such as Cuculus and Eo-Oligocene of France (Weigel 1963), some Chrysococcyx,exhibit egg polymorphism, egg workerssuggest that the cuckoosdiverged from mimicry and egg crypsis--traditionallyattrib- ancestralstock during the Late Cretaceous(Sib- uted to an extended coevolutionary relation- ley and Ahlquist 1990). Fundamental differ- 10 January1996] CuckooPhylogeny Based on Behavior ences in external and internal morphology TABLE 1. Classification of the Cuculiformes sensu within the group have perplexed systematists Peters(1940). Obligately parasiticgenera indicated with asterisk(*). Facultatively parasitic genus in- for decadesand, althoughproblematic, the most dicatedwith diamond(0). acceptedclassification of the cuckoosis that of Peters(1940), which is basedpredominantly on Order Cuculiformes breeding habits and geographic distribution Family Musophagidae (Table 1). Several alternate classificationsof the Family Cuculidae Subfamily Cuculinae Cuculidaehave been proposedin past decades Genus Clamator* followingthe anatomicalstudies of Berger(1952, GenusPachycoccyx* 1954, 1960) and Verheyen (1956a), and more Genus Cuculus* recentlyby Sibleyand Monroe (1990)based on Genus Cercococcyx* Genus Penthoceryx* DNA-DNA hybridization of Sibley and Ahlqu- Genus Cacomantis* ist (1990). However, these studies have not Genus Rhamphomantis* gained wide acceptanceand, as a result, most Genus Misocalius* current classifications still adhere to the se- Genus Chrysococcyx* Genus Chalcites* quencein Peters(1940). Phylogeneticsystem- Genus Caliechthrus* atics had not been used to constructa hypoth- Genus Surniculus* esis of evolutionary relationship among the Genus Microdynamis* cuckoosuntil Seibel (1988) addressedthe family GenusEudynamys* in a cladisticanalysis of postcranialosteological Genus Urodynamis* characters.Not surprisingly,his resultsdid not Genus Scythrops* Subfamily Phaenicophaeinae entirely supporttraditional classifications of the GenusCoccyzus• group. Regrettably, this work remains in dis- Genus Hyetornis sertationform only and, hence,has not received Genus Piaya Genus Saurothera criticalattention from the scientificcommunity. Genus Ceuthmochares The considerationof behavior and ecology Genus Rhopodytes has often been used to evaluate the evolution- Genus Taccocua ary relationshipsamong birds (e.g. Whitman Genus Rhinortha 1899,Heinroth 1911,Davis 1942,Mayr and Bond Genus Zanclostomus Genus Rhamphococcyx 1943, Tinbergen 1959, Strauch 1985, Prum and Genus Phaenicophaeus Johnson 1987, Prum 1990). More specifically, GenusDasylophus Baker (1927), Bannerman (1933), and Delacour Genus Lepidogrammus (1947) suggestedthat the cuckooscould be sub- Subfamily Crotophaginae Genus Crotophaga divided basedon their breeding habits. In ad- Genus Guira dition, Delacour and Mayr (1946) noted that Subfamily Neomorphinae habitat use may be a valid systematiccharacter Genus Tapera* for determining some degree of relationship Genus Morococcyx within the family. In the present study, ! use GenusDromococcyx* 28 behavioral and ecologicalcharacteristics to Genus Geococcyx Genus Neomorphus reconstructthe evolutionaryrelationships of the GenusCarpococcyx Cuculidaeby phylogeneticsystematics. The re- Subfamily Couinae suiting topologiesdiffer significantly from tra- Genus Coua ditional classifications of the cuckoos in both Subfamily Centropodinae Genus Centropus placement and membership of subfamilies. Basedmy resultsand other evidence,! propose a new hypothesisfor the evolution of brood parasitismin this taxon. broadlyas those representing movement of all or part of the external anatomyof the bird and, therefore, encompassa numberof functionalcategories such as METHODS socialinteraction, courtship, nest building, egg lay- ing, and incubation. Several ecologicalcharacters Data.--Twenty-eight behavioral and ecological comprisingdiet and habitatuse alsowere included. characterswere used (seeAppendix 1 for character Data were collected for 38 genera of cuckoos,the descriptions).As suggestedby De Queiroz and Wim- turacos(Musophagidae), and the Hoatzin (Opistho- berger (1993), behavioral characterswere defined comushoatzin) through an extensiveliterature search 12 JANICEM. HUGHES [Auk,Vol. 113 TABLE2. Data matrix of behavioral and ecologicalcharacters for Musophagidae,Opisthocomus hoatzin, and 21 generaof Cuculidae(see Appendix 2 for characterdefinitions). Missing data indicatedby "". Genera markedwith asterisks(*) areobligate parasites; genus marked with diamond(¸) is facultativelyparasitic. Character Taxon 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 Musophagi- dae 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Opisthocomus0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 0 0 0 Clamator* 0 1 1 1 1 1 1 1 1 1 0 3 3 1 0 1 1 1 3 1 0 0 1 0 0 0 1 0 Pachgcoccgx* 0 1 1 0 1 0 3 1 0 1 0 3 3 0 1 1 1 1 3 1 1 1 1 0 0 0 1 0 Cuculus* 0 1 1 1 1 0 2 1 0 0 1 3 3 0 1 1 3 2 3 1 1 1 0 0 0 1 1 0 Cacomantis* 0 1 1 1 0 0 0 1 0 ? ? 3 3 0 1 1 2 2 3 1 1 1 0 0 0 1 1 0 Chrgsococcgx*0 1 1 1 1 0 1 1 0 1 1 3 3 0 1 1 1 2 3 1 1 1 1 0 0 1 1 0 Misocalius* 0 1 1 1 0 0 1 1 0 ? ? 3 3 0 1 1 2 1 3 1 1 1 0 1 0 0 1 0 Chalcites* 0 1 1 1 1 0 1 1 0 1 1 3 3 0 1 1 3 2 3 0 1 1 0 0 0 1 1 0 Eydynamys* 0 1 0 1 0 0 0 1 ? 0 0 3 3 1 0 1 1 1 3 1 1 0 0 0 0 0 1 0 Scythrops* 0 1 0 1 0 0 0 1 0 ? ? 3 3 0 0 1 1 1 3 1 1 0 0 0 0 0 1 0 Cocc!/zus• 0 1 1 1 1 0 0 0 0 0 1 0 1 0 0 1 2 1 0 1 0 0 0 0 0 0 1 0 Piaya 0 1 2 0 0 1 0 0 0 0 ? 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 Saurothera 1 0 3 0 0 0 0 0 ? 0 ? 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Crotophaga 0 0 2 0 0 2 0 0 1 0 0 1 0 0 0 1 0 1 0 0 1 0 0 0 0 0 0 0 Guira 0 0 2 0 1 2 0 0 1 0 0 1 0 0 0 1 0 1 0 0 1 0 0 0 0 0 0 0 Tapera* 1 0 2 0 0 0 0 ? ? 1 1 3 3 0 0 1 2 2 3 0 0 0 0 1 0 0 1 0 Morococcyx 1 0 2 0 0 0 0 ? ? 0 ? 1, 2 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 Neomorphus 1 0 3 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 Geococcyx 1 0 3 0 0 0 0 0 0 0 1 0 1 0 0 0 0 0 1 0 0 0 0 0 1 0 0 0 Carpococcyx 1 0 3 0 0 0 0 0 ? 0 1 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 Coua 1 0 3 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 Centropus 1 0 3 0 1 1 2 0 1 0 1 2 1 0 0 0 0 0 2 0 0 0 1 0 0 0 0 1 (Appendix 2).
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