The Auk 110(4):798-824, 1993 INTERGENERIC PHYLOGENETIC RELATIONSHIPS OF SWALLOWS ESTIMATED BY DNA-DNA HYBRIDIZATION FREDERICK H. SHELDON 1 AND DAVID W. WINKLER 2 •Departmentof Ornithology,Academy of Natural Sciences, 1900Benjamin Franklin Parkway, Philadelphia, Pennsylvania 19103, USA; and 2Sectionof Ecologyand Systetnatics,Division of BiologicalSciences, CorsonHall, CornellUniversity, Ithaca, New York 14853, USA ABSTRACT.--Thephylogeny of the subfamily Hirundininae was estimatedby hybridizing single-copynuclear DNAs of 21 swallow species,representing 19 former and current genera, and a Tufted Titmouse(Parus bicolor) as outgroup.The phylogeny, which was unusually well resolved, consisted of three fundamental clades: Hirundo and allies, core martins, and African sawwings.The clade of Hirundoand allies comprisedHirundo rustica, Ptyonoprogne fuligula, Delichonurbica, Cecropis semirufa, Petrochelidon pyrrhonota, and P. spilodera.The sister-groupof Hirundoand allies was the core martin clade, which consistedlargely of endemic New World taxa (Pygochelidoncyanoleuca, Neochelidon tibialis, Atticora fasciata, Phaeoprogne tapera, Progne chalybea,Haplochelidon andecola, Stelgidopteryx ruficollis, and Tachycinetabicolor) and somebasally branchingOld World groups(Riparia riparia, R. cincta,Phedina borbonica, Pseudhirundo griseopyga, and Cheramoecaleucosternus). The African sawwings (represented by Psalidoprocneholomelas) formed the sister group of the core martins and Hirundoand allies. Among some interesting discoveries,we found a close relationship between the monotypic African and Australian generaPseudhirundo and Cheramoeca.We also found that Delichon,which has persistedin the nomenclatureas a genusseparate from Hirundo,is monophyleticwith taxathat are commonly considered to be members of Hirundo. On the other hand, Haplochelidonandecola, which is often considered to be a Hirundo or Petrochelidon,is not closely related to those genera, but instead lies among the New World membersof the core martin clade. Received1 July 1992, accepted25 November1992. PERHAPSNO FAMILY of passerinesis asuniform titude of small, seemingly equally divergent morphologicallyand diverse genericallyas the genera had been defined mainly on the basis swallows (Hirundinidae). All swallow species of external morphological characters (e.g. conform to a fundamental body plan that in- plumage color, nasal form, fusion of skin be- cludeslong and pointedwings, mediumlength tween toes,tarsal feathering, and size).To bring tails, short legs, and bills that are short and someorder and logic to this confusingarray of wide. This uniformity is the likely resultof ad- names, Mayr and Bond grouped swallow gen- aptation to a strictly aerial insectivorouslife- era into units using what they consideredto be style. Apparently becauseof this uniformity, conservative, phylogenetically informative systematistshave been loath to attempt a phy- characteristics,in particular those of nesting logeneticreconstruction of the swallow family habits and plumage color patterns. In the pro- as a whole. While there have been many clas- cess,they outlined a rough scenarioof swallow sificationsof the Hirundinidae (e.g. Sharpe1885, evolution based on nesting strategy and to a Peters 1960, Turner and Rose 19•9, Sibley and lesser extent geography. They postulated that Monroe 1990)and many discussionsof the sys- the most "primitive" species were those that tematics of individual speciesor small groups nested in natural cavities or on ledges. These of taxa, only one publishedpaper has consid- were followed in evolutionary sequenceby spe- ered the familywide relationshipsof swallows ciesthat excavatednest holes and finally species based on evolutionary or phylogenetic logic. that built nests from mud. Old World groups This is the 50-year-oldstudy of Mayr and Bond were judged to be more primitive than New (1943). World taxa because Africa, as the continent with At the time of Mayr and Bond's (1943) study, the most swallow species,was perceived as the some 30 to 35 generic nameshad been applied center of their origin. In addition to behavioral to the 75 to 80 speciesof swallows. This mul- and geographic criteria, some features of exter- 798 October1993] SwallowPhylogeny 799 T^nLE1. List of commonly used generic names of portance of historical components to modern swallows and examples of synonymy. Current behaviorand ecology(e.g. Ricklefs1987, Brooks names taken from Sibley and Monroe (1990). Syn- onyms from Roberts(1922), Hellmayr (1935), Peters and McLennan 1991), further understanding of (1960), Brooke (1974), AOU (1983), and Turner and the phylogeny of this group seems especially Rose (1989). warranted. In the present paper, we reexamine the re- Alternative or subsumed lationships among genera of the Hirundininae Current name general names using genetic information derived from DNA- Tachycineta Iridoprocne,Callichelidon, Kalo- DNA hybridization. This independent source chelidon,Lamprochelidon of genealogical information has generated a Phaeoprogne -- Progne Phaeoprogne phylogenetic hypothesisthat can be used to test Notiochelidon Orochelidon,Pygochelidon the schemeof Mayr and Bond (1943), as well as Atti•:ora Diplochelidon serve as a template for analyses of character Neochelidon -- evolution in this popular group. Stelgidopteryx Alopochelidon Cheramoeca -- Riparia Neophedina,Cheimonornis METHODS Phedina Phedinopsis Hirundo Pseudhirundo,Ptyonoprogne, Selectionof taxa.--The speciesused in our study and Cecropis,Petrochelidon, Nata- sources of tissues for DNA extraction are listed in lornis, Charitochelidon,Phoeni- Table 2. While the taxonomic order of this list follows chelidon,Baruwaia, Haplo- Sibley and Monroe (1990), we have employed gen- chelidon erally older generic namesto clarify our discussion, Delichon particularly of taxa that are now commonly lumped Psalidoprocne in Hirundo. All of the specieslisted in Table 2 are members of the subfamily Hirundininae (true swal- lows). The other swallow subfamily Pseudochelidoni- nal morphology (e.g. wing serrations of saw- nae (river-martins) consistsof only two species,one wing or rough-winged swallows) were used to from central Africa (Pseudochelidoneurystomina) and define evolutionary advancement. one (possibly extinct) from Thailand (P. sirintarae). Unfortunately, we did not have DNA from either of Although openly preliminary, Mayr and these species. Bond's (1943) treatment remains the most in- In choosingtaxa for comparison,we tried to include fluential effort to date, supplying the rationale representativesof as many previously recognized behind the linear arrangementof swallow spe- genera as possible, especially those whose relation- ciesin mostclassifications. Under its logic, many ships remain obscure.We also included representa- of the old generic names have been subsumed tives of all the groups defined by Mayr and Bond (e.g. see Table 1), so that only 10 to 20 genera (1943). Here we summarizetheir groupsand list the are commonly recognized today (Brooke 1974, speciesin each that we compared. Mayr and Bond Bock and Farrand 1980, AOU 1983, Turner and (1943) divided Hirundointo three subgenera:(1) sub- Rose 1989, Sibley and Monroe 1990). However, genus Hbundo, cup-nesting barn swallows (Hirundo rustica)and crag martins (Ptyonoprognefuligula); (2) we still have no idea how thesemodern genera subgenusLillia, rufous-rumped, retort-nest builders fit together phylogenetically, or whether Mayr (Cecropissemirufa); and (3) subgenusPetrochelidon, cliff and Bond's evolutionary |ogic and choice of swallows (Petrochelidonpyrrhonota and P. spilodera). characters have merit. House martins (Delichon urbica) were viewed as "an The uncertainty of relationships among hi- obvious descendant of Petrochelidon"(p. 335). Sepa- rundines could well serve as sufficient justifi- rate from Hirundo and allies, Mayr and Bond distin- cation for further systematic research on the guisheda seriesof hole-nestinggroups: (1) bank-mar- group. The inherent interestin their genealogy tins (Ripariariparia, R. cincta),basically an Old World is strengthened because swallows are among group of four speciesthat excavatetheir own burrows; the most popular subjectsfor behavioral and (2) rough-winged swallow group (Stelgidopteryxruff- coilis,Neochelidon tibialis ), generally dull-colored,New ecologicalresearch in ornithology. Every year, World birds that nest in crevices or burrows excavated dozens of papers are published on the field bi- by otherspecies; (3) the Atticoragroup (Atticora fasciata, ology of several North Temperate species, es- Pygochelidoncyanoleuca), generally blue Neotropical pecially Hirundorustica, Petrochelidon pyrrhonota, taxa that nest mainly in crevices; (4) tree-swallow Delichonurbica, Tachycineta bicolor, and Progne group (Tachycinetabicolor), New World tree-hole subis.Given the growing awarenessof the im- adopters;and (5) purple-martin group (Prognesubis, 800 SHELDONAND WINKLER [Auk, Vol. 110 October1993] SwallowPhylogeny 801 Phaeoprognetapera), another group of New World hole (HAP) columnsplaced in a thermal-elution device adopters.Mayr and Bondalso identified severalprob- similar to those of Sibley and Ahlquist (1981) and lematic taxa that did not fit well into any of these Kirschet al. (1990).Fractions of swallow/swallowhy- categories.Of these, we comparedthe Australian brids were taken at 60øC and 72 ø to 94øC in 2.0øC White-backed Swallow (Cheramoecaleucosternus), Af- incrementsby pumping 4 ml of 0.12 M sodiumphos- ricanGrey-rumped Swallow (Pseudhirundo griseopyga),