The Condor 971492-502 0 The CooperOrnithological Society 1995

PHYLOGENETIC RELATIONSHIPS AMONG NORTH AMERICAN INFERRED FROM RESTRICTION ENDONUCLEASE ANALYSIS OF MITOCHONDRIAL DNA ’

DARRELL L. ELLSWORTH,~ RODNEY L. HONEYCUTT AND NOVA J. SILVV Department of Wildlif and Fisheries Sciences, Texas A&M University, College Station, TX 77843

Abstract. Systematic relationshipsamong North American grouseand ptarmigans(Te- traoninae) are not well defined becausetraditional classificationswere based on morpho- logicaland behavioral characterswith limited taxonomic utility. Restriction enzyme analysis of mitochondrial DNA (mtDNA) was used to generate a phylogeny for North American tetraonines that was then utilized to test previous phylogenetic hypothesesfor the group and to examine the origin and of complex reproductive behaviors and morpho- logical features characteristicof grouseand ptarmigan .Nucleotide sequencediver- genceamong congenericspecies derived from mtDNA restriction fragment patterns varied extensively, ranging from 0.28% in prairie grouse () to 4.06% among ptar- migans () and 10.15% between Blue Grouse ( obscurus) and (0. canadensis). Using the ( virginianus) as an outgroup, the molecular phylogeny partitioned speciesinto three primary groups:(1) Tympanuchus; (2) Lagopus, Dendragapus obscurus, and Tetrao urogallus (the European Capercaillie);and (3) the (Bonasa umbellus), Dendragapus canadensis, and SageGrouse (Cen- trocercus urophasianus). Prairie grousewere genetically distinct from other grousespecies, but a polyphyletic distribution of haplotypes and limited mtDNA differentiation within Tympanuchus suggestthat divergence among the prairie grouse occurred very recently. Within Lagopus, the (L. lagopus) and Rock (L. mutus) Ptarmiganswere more closely relatedto eachother than eitherwas to the White-tailedPtarmigan (L. leucurus). Dendra- gapus canadensis groupedwith Bonasa umbellus; whereasD. obscurus was allied with La- gopus and Tetrao. Thus, the genus Dendragapus as currently constructedis polyphyletic (i.e., D. canadensis and D. obscurus have had separateevolutionary histories)and the mor- phologicalsimilarities between the two speciesmay be attributable to convergentadaptation to coniferous . We inferred from the molecular phylogeny that the complex repro- ductive systemsin tetraonines have arisen independently and that correspondingmorpho- logical and behavioral specializationsmay reflect parallel evolutionary trends. Key words: Tetraoninae; grouse; ptarmigans; mtDNA; systematics; evolution.

INTRODUCTION , , , , , Grouse and ptarmigans comprise a group of gal- and Old World (Sibley and Ahlquist 1990). liform that collectively have a circumpolar Previous classifications of grouse and ptar- distribution in the Northern Hemisphere. There migan specieshave been derived from subjective are currently ten recognized speciespartitioned evaluations of morphological characters(such as into five genera in North America. Traditionally, natal , color, number of rectrices) grouse and ptarmigans have been viewed as a and behavioral patterns associated with court- distinct family (Tetraonidae) on the basis of mor- ship display (Short 1967, Fjeldsa 1977, Johns- phological features such as feathered tarsi and gard 1983, Potapov 1985). Morphological and nostrils and pectinate toes (Peters 1934, Ridgway behavioral similarities among taxa may result and Friedmann 1946, Wetmore 1960). However, from homology (a common ancestry) or analogy the Tetraonidae has been relegatedto subfamilial (derived from independent evolution toward a status (Tetraoninae; Brodkorb 1964, Holman common function); however, only homologous 1964) within the along with pheas- characters provide reliable information for re- constructing evolutionary relationships. The an- atomical and behavioral features utilized in the classification of grouseand ptarmigans have lim- I Received20 July 1994.Accepted 17 January 1995. 2 Presentaddress: Human GeneticsCenter, Univer- ited taxonomic utility becausethey: (1) are adap- sity of TexasHealth ScienceCenter, P.O. Box 20334, tive and subject to convergent evolution; (2) tend Houston,TX 77225, USA. to evolve rapidly in avian species(Johnston and

WV SYSTEMATICS OF NORTH AMERICAN GROUSE 493

Selander 1964); and (3) may have an environ- (L. mutus) n = 3; Greater Prai- mental (non-genetic) component influencing their rie-chicken (Tympanuchus cupido) n = 6; Lesser expression. As a result, the classifications based Prairie-Chicken (T. pallidicinctus) n = 5; and on such characteristics differ greatly in topology Sharp-tailed Grouse (T. phasianellus) n = 7. A and tend to contain monotypic genera. European grouse, the Capercaillie (Tetrao uro- Grouse and ptarmigans exhibit complex social gallus, n = l), was included in the analysis and behaviors and anatomical specializations that are the Northern Bobwhite (Colinus virginianus, n associated with unique life history and repro- = 1) was used as an outgroup. Detailed infor- ductive strategies, including monogamy and sev- mation regarding collecting localities is present- eral distinct types of polygyny (Oring 1982; ed in Appendix 1. Johnsgard 1983, 1994). Many species are sexu- Mitochondrial DNA from 54 individuals was ally dimorphic and dichromatic, with a variety isolated from frozen tissue and purified on ce- of novel behaviors (ritualized postures, vocali- sium chloride density gradients (Car-r and Grif- zations, aerial displays) and morphological char- fith 1987). We digested aliquots of purified acteristics (inflatable esophageal air sacs, mtDNA with 14 restriction enzymes: Apa I, specializations) present in males. Reproductive BumH I, Bcl I, Cla I, Hind III, Hpa I, Kpn I, systems in grouse and ptarmigans have been in- Nco I, Nde I, Pst I, Pvu II, Sal I, Sst I, and Xba tensively studied; however, there is currently no I. The resulting fragments were end-labeled with solid framework (a phylogeny derived from in- @P-nucleotide triphosphates using DNA poly- dependent characters) on which to interpret and merase (Klenow fragment), separated on 1.2% analyze the evolution of these complex behav- vertical agarose gels, and visualized by autora- ioral patterns and morphological features. diography. Fragment sizes were estimated by di- Genetic approaches have facilitated our ability rect comparisons with co-migrating standards of to make inferences about evolutionary relation- known size (a mixture of lambda DNA and PM2 ships among birds. Analyses of mitochondrial DNA digested with Hind III). DNA (mtDNA) have proven to be particularly For each restriction enzyme, we assumed that useful for determining systematic relationships fragments exhibiting identical mobilities were among species (Kessler and Avise 1984, Oven- homologous (i.e., attributable to the same re- den et al. 1987, Gill and Slikas 1992) and for striction sites across taxa). To minimize the pos- differentiating morphologically similar taxa sibility of scoring nonhomologous fragments of (Mack et al. 1986, Avise and Nelson 1989). In similar size as identical due to indistinguishable this paper, restriction endonuclease analysis of differences in migration, bands of questionable mtDNA was used to examine the evolutionary size identity were compared side-by-side on 1% affinities of all North American grouse and ptar- vertical agarose gels. Fragments that appeared to migan species. Our study: (1) tests previous phy- be similar in size on 1.2% gels, but which could logenetic hypotheses derived from morphology, be differentiated on the 1% gels, were labeled plumage, and behavior with a molecular data set; alphabetically (e.g., 800a and 800b) and treated (2) clarifies the origin and evolution of complex as separate fragments (Appendix 2). However, reproductive systems and associated morpho- certain enzymes produced only one fragment in logical/behavioral traits in tetraonines; and (3) several different species. We determined whether contributes to our understanding ofthe evolution these fragments were homologous (attributable of grouse and ptarmigan species. to the same site) or nonhomologous (attributable to different sites) by digesting the sample with a METHODS second restriction enzyme that cut the DNA only Brain and/or liver samples were collected from at sites known to be identical in all taxa. If the specimens distributed throughout the geographic fragments were homologous, identical profiles range of all North American grouse and ptar- were observed in the double digests. Fragments migans as follows: Ruffed Grouse (Bonasa um- deemed nonhomologous by the double diges- bellus) n = 6; Sage Grouse ( uro- tions were also treated as different fragments. ) n = 6; Spruce Grouse (Dendragapus Each individual was scored for the presence or cunadensis) n = 6; Blue Grouse (D. obscurus) n absence of each restriction fragment and assigned = 4; (Lagopus lagopus) n = a composite haplotype based on fragment pro- 7; White-tailed Ptarmigan (L. leucurus) n = 4; files across all restriction enzymes. The propor- 494 D. L. ELLSWORTH, R. L. HONEYCUTT AND N. J. SILVY

tion of shared fragments (F; Nei and Li 1979) was used to estimate the extent of nucleotide I sequence divergence (P) among the composite haplotypes. We then determined the phyloge-

N netic relationships among speciesfrom the ma- hOO I N. trix ofP-values using the FITCH (with GLOBAL -Q\ optimization and RANDOM addition of taxa) and NEIGHBOR options in PHYLIP (Felsen- stein 1989). The FITCH algorithm uses Fitch- Margoliash (Fitch and Margoliash 1967) and least-squares methodology (Cavalli-Sforza and Edwards 1967) to construct a phylogenetic net- work. NEIGHBOR implements the distance ma- trix (Neighbor-Joining) method of Saitou and Nei (1987) to infer a tree that may have the smallest sum of branch lengths. Neither approach as- sumes that rates of genetic change are uniform among lineages.

RESULTS Fragment profiles and co-migrating size stan- dards were used to estimate the length of the mtDNA molecule in Tetraonines to be approx- imately 16.6 kb, which is typical for many avian species(Shields and Helm-Bychowski 1988). All individuals possesseda single mtDNA haplotype and no length variation due to insertions or de- letions was detected. The restriction enzyme analysis produced 248 unique fragments comprising 24 composite mtDNA haplotypes (Appendix 2). Estimates of nucleotide sequence divergence among haplo- types within specieswere generally lessthan 1.OO (Table 1). However, a divergent lineage of Den- dragapus obscurusfrom Vancouver Island dif- fered from other conspecificpopulations in Col- orado and Montana by 1.45%. No mtDNA vari- ation was detected in the Centrocercusurophas- ianus samples obtained from California, Colorado, and . Estimates of mtDNA differentiation among congenericspecies varied extensively. Within the Tympanuchuscomplex we identified 4 mtDNA haplotypes, but they were not strictly partitioned along speciesboundaries. Two of the haplotypes were unique to T. cupido (No. 19 and No. 20), one haplotype was shared by T. cupido and T. pallidicinctus (No. 21), and one haplotype was common to all three species(No. 22) (Appendix 2). Sequencedivergence among the prairie grouse haplotypes (maximum differentiation = 0.40%) was equivalent to or less than the divergence estimates observed within other speciesof North SYSTEMATICS OF NORTH AMERICAN GROUSE 495

c - 2.98 Bonasa umbellus

1.60

0.59 3.87 11 Dendragapus canadensis

2.17 Centrocercus urophasianus

1.17r Lagopus lagopus 0.95 1.64 r I 1.47 -Gl Lagopus mutus 0.28 \ 1.65 [ Lagopus leucurus

_ 1.43 t-c Dendragapus obscurus - 0.16 5.21 Tetrao urogallus

1.35 Tympanuchus spp. -\ I

11.78 Colinus virginianus FIGURE 1. Fitch-Margoliashtree (average %SD = 9.99)derived from a matrixof mtDNA sequencedivergence valuesdepicting evolutionary relationships among all speciesof North Americangrouse and ptarmigans.Branch lengthswithin specieswere generally < 1 and arenot shown.The treeis “rooted” by the outgrouptaxon, Colinus virginianus.

American grouse. Differentiation among the only slightly exceededthe maximum estimate of ptarmigan species(Lagopus) ranged from 3.3 1% differentiation among the grouse taxa (11.84%); to 5.13%. In contrast to both Tyrnpanuchus and and (3) odontophorines are related to tetraonids Lagopus, the two speciesof Dendragapus (can- by a variety of morphological and behavioral adensis and obscurus) differed by 10.15%, one of characteristics(Johnsgard 1973). the highest P-values observed between any pair Trees derived by the Fitch-Margoliash (Fig. 1) of taxa (including the intergeneric comparisons). and Neighbor-Joining (Fig. 2) algorithms were Mitochondrial DNA sequencedivergence be- identical in overall topology. Both methodolo- tween Colinus and the various grouse species giespartitioned speciesinto three primary groups: rangedfrom 13.45%~~. Tympanuchusto23.91% (1) Tympanuchus; (2) Lagopus, Dendragapus ob- vs. Dendragapus canadensis. We believe C. vir- scurus, Tetrao urogallus; and (3) Bonasa umbel- ginianus was an appropriate outgroup because: lus, Dendragapus canadensis, Centrocercus uro- (1) all of the outgroup-&group comparisons ex- phasianus. Members of the genus Tympanuchus ceededthe estimatesof differentiation among the fall outside the group containing all other North grousespecies indicating that Colinus lies outside American grouse and ptarmigans. Bonasa um- the Tetraoninae; (2) a was not bellus and Dendragapus canadensis group to- too distant to provide useful outgroup infor- gether, and Centrocercus appears to be affiliated mation because the minimum level of mtDNA with Bonasa and D. canadensis but the associ- divergence between Colinus and grouse(13.45%) ation is relatively weak. The fragment analysis 496 D. L. ELLSWORTH, R. L. HONEYCUTT ANDN. J. SILVY

Bonasa umbellus

DP . c1Dendragapus canadensis ADP I Centrocercus urophasianus

_I Lagopus lagopus

M Lagopus mutus + --I!1

1 Lagopus leucurus DP < Dendragapus obscurus PID I Tetrao urogallus

ADP -11Tympanuchus spp. M I Colinus virginianus FIGURE 2. Network of relationshipsfor North American grouseand ptarmigansbased on the Neighbor- Joiningmethod (Saitou and Nei 1987).The branchingpattern of the Neighbor-Joiningtree is identicalto that of the Fitch-Margoliashnetwork (Fig. l), but branch lengths differ slightly. Mating systemsof the taxa under consideration are plotted on the tree (M = monogamy, DP = dispersedpolygyny, PID = polygyny with inter- mediatedispersion, ADP = arenadisplay polygyny). _ partitioned the ptarmigans into a single clade and causetheir plumage differs extensively from oth- resolved relationships among species that are er species(being almost entirely barred) and males consistent with previous classifications (Short possessnumerous morphological structures as- 1967, Fjeldsa 1977, Johnsgard 1983). Tetrao and sociated with complex courtship (lekking) be- D. obscurusare included in the group with La- havior (Johnsgard 1983, 1994). Tympanuchus gopus; however, the branches defining these re- cupido and T. pallidicinctus are recognized as lationships are relatively short. Nevertheless, our distinct species(American Ornithologists’ Union phylogeny indicates that Dendragapus canaden- 1983); however, the differences (in behavior, sis and D. obscurus,which are currently consid- habitat, and social aggregation) that distinguish ered congeneric, have had separateevolutionary these taxa (Grange 1940, Jones 1964, Sharpe histories. 1968) are relatively minor compared to those observed between other well-defined species. Thus, some researchers(Short 1967, Johnsgard DISCUSSION 1983) consider T. cupido and T. pallidicinctus GENUS TYMPANUCHUS allopatric subspecies. Tympanuchus phasianel- (PRAIRIE GROUSE) lus (formerly Pedioecetesphasianellus) was once Prairie grouseare adapted to grasslandand grass- placed in a separategenus due primarily to dif- land-woodland ecotone throughout the central ferences in morphology (Ridgway and Fried- and Canada. Prairie grouse are mann 1946) but Pedioeceteshas been synony- considered to be distinct from other genera be- mized with Tympanuchus(Short 1967). SYSTEMATICS OF NORTH AMERICAN GROUSE 497

The mtDNA fragment data suggestthat Tym- Tetrao, and Dendragapus obscurus is evident in panuchus is distinct at the generic level. How- the mtDNA phylogeny, but relationships among ever, the extent of interspecific differentiation was these taxa are not confidently resolved. far less than that observed between other con- generic grouse species (such as Lagopus) and ap- DENDRAGAPUS, A POLYPHYLETIC proximated the lowest mtDNA distances seen GENUS among closely related avian species (Avise and The range of D. obscurus is closely associated Zink 1988). A second striking aspect of mtDNA with the distribution of true and differentiation within Tympanuchus was the ob- in western North America (Beer 1943); whereas, servation that several haplotypes were shared D. canadensis occurs transcontinentally in boreal among species. Ellsworth et al. (1994) examined coniferous (Aldrich 1963). From 1899 mtDNA variation in Tympanuchus and con- until 1967, D. canadensis (formerly Canachites cluded that the low level of interspecific diver- canadensis) and D. obscurus were placed in dif- gence and polyphyletic distribution of haplo- ferent genera. Short (1967) merged Cunachites types is most likely attributable to recent speci- with Dendragapus on the basis of similarities in ation, possibly resulting from subdivision caused overall body proportions, bill, wing, and tail by Pleistocene glacial activity. morphology, egg color, and juvenile plumage. In GENUS LAGOPUS, THE PTARMIGANS this study, D. canadensis and D. obscurus were among the most genetically divergent tetraonine Ptarmigans are small to medium sized grouse taxa in North America. Relationships inferred that inhabit tundra and alpine habitats. Features from molecular characters indicate that these two distinctive of Lagopus such as feathered toes with species do not constitute a monophyletic lineage. reduced lateral pectinations and multiple com- Dendragapus canadensis groups with Bonasa plex molts generally reflect adaptation to cold umbellus, but D. obscurus is affiliated with La- northern environments. Lagopus lagopus and L. gopus and Tetruo. Thus, the morphological sim- mutus are sympatrically distributed in the tundra ilarities between the species may be attributable and northern boreal forests of the Holarctic; to convergent evolution associated with adap- whereas, leucurus is restricted to high altitude tation to coniferous forest habitats. regions in western North America (Johnsgard 1983). There is controversy surrounding the phylo- EVOLUTION OF TETRAONID MATING genetic relationships of ptarmigans; two oppos- SYSTEMS ing classifications have been proposed. Plumage, Grouse and ptarmigans exhibit a variety of com- egg color, and the progression of molts may sug- plex reproductive systems, ranging from nearly gest that L. leucurus diverged prior to the sepa- monogamous to polygynous (male-dominance). ration of L. lagopus and L. mutus (Short 1967, Male ptarmigans establish large territories and Hiihn 1980, Johnsgard 1983). However, behav- usually form a pair bond with only one female ioral patterns have been interpreted as evidence (Johnsgard 1983), but in the polygynous species that L. lugopus was the earliest divergent lineage males mate with several females by overtly com- (Johansen 1956, Braun 1969). The mtDNA data peting with one another by ritualized display. support the classification of Short (1967) that The polygynous mating systems are divisible into places L. lagopus and L. mums as being more three types based on the degree of male clustering closely related to each other than either is to L. during reproductive competition (Oring 1982): leucurus. (1) dispersed polygyny where males occupy large Tetruo urogullus, the largest member of the and widely spaced territories is typical of the grouse family, occupies coniferous forests in Eu- forest dwelling grouse (Dendragapus canadensis, rope and Asia (Johnsgard 1983). Based primarily D. obscurus, and Bonasa umbellus) (Lumsden on similarities in female and natal plumage and 1968, Hjorth 1970); (2) intermediate dispersion, the frequency of hybridization, Short (1967) con- exemplified by Tetrao urogallus, in which males sidered Lagopus and Tetrao to comprise a major display from sites that are markedly clumped; monophyletic lineage of grouse that exhibits more and (3) the complex arena display of Centrocer- distant affinities with Dendragapus (D. canaden- cus and Tympanuchus where males aggregateand sis in particular). An association among Lagopus, aggressively defend small display territories 498 D. L. ELLSWORTH, R. L. HONEYCUTT ANDN. J. SILVY known as leks (Hamerstrom and Hamerstrom independently in these taxa; (2) the display be- 1973, Ballard and Robe1 1974). haviors and morphological specializations in Other galliform groups such as and par- males that are associatedwith reproduction are tridges retain a strongly monogamous system; attributable to parallel evolutionary trends; and thus monogamy in the ptarmigans is believed to (3) such displays are not homologous characters representan ancestralcondition. The polygynous and similarities between reproductive systems systemsin the other grousespecies were believed do not imply phylogenetic relatedness. to be independently derived (Short 1967, Johns- MITOCHONDRIAL DNA RESTRICTION gard 1983); however, this hypothesis could not FRAGMENTS FOR PHYLOGENETIC be critically tested because systematic relation- ANALYSIS shipsamong tetraonines were based primarily on Although restriction sites are often more infor- similarities for morphological and behavioral mative than fragments, concurrent analyses of charactersthat are closely associatedwith repro- fragments and siteshave produced congruent re- duction. sults in several systematicstudies involving birds Relationships among taxa suggestedby the (Zink 199 1, Zink and Dittmann 199 1, Gill and mtDNA analysis allow us to make preliminary Slikas 1992). Additionally, the average P-values inferences regarding the evolution of the various for all pairwise comparisons among the grouse reproductive systems in grouse and ptarmigans and ptarmigan species(Table 1) were less than using a phylogeny derived from independent 12%, which is below the 15% maximum diver- characters.The molecular data are consistentwith gence suggestedby Upholt (1977) and Dowling the independent origins of both the dispersed et al. (1990) for fragment comparisons. The pro- polygynous and communal display behaviors portion of fragments shared by at least two in- (Fig. 2). For example, Bonasa umbellusand Den- group taxa (41%) was also far greater than the dragapus canadensisshare the dispersed polyg- minimum level (25%) proposed by Kessler and ynous system with D. obscurus.All three species Avise (1985). are adapted to northern coniferous or deciduous Our phylogeny for the Tetraoninae based on forest. Dendragapus males make aerial display mtDNA restriction fragments is a preliminary flights in which “clapping” or “drumming” of estimation of the evolutionary affinities among the wings may occur (Blackford 1963, MacDon- grouseand ptarmigans. Resolution was sufficient ald 1968). Bonasa males also establish territories to confidently discern relationships (or lack and advertise for mates with a drumming dis- thereof) among congeneric species, to evaluate play, but extensive wing beating has been sub- the phylogenetic significance of current taxo- stituted for flight (Hjorth 1970). In our phylog- nomic groupings, and to make inferences re- eny, B. umbellus and D. canadensisgroup to- garding the evolution of mating systemsand se- gether; whereas, D. obscurusis genetically dis- lected morphological traits. However, several tinct. Thus, the development of dispersed problematic areas such as the interrelationships polygyny and similarities in male courtship that among several primary lineages and the place- B. umbellus and D. canadensisshare with D. ob- ment of other tetraonid speciesremain. scurusmight reflect selective pressuresunique to northern forest environments. ACKNOWLEDGMENTS Similarly, Centrocercusand Tympanuchusare We thank the following individuals for collectingtissue lek-forming taxa that occupy open shrubland/ samples: E. , N Steen, Alaska Department of grassland habitats in central and western North Fish and Game: J. Cauodice. Bureau of Land Man- America. Males advertise to attract females with agement;B. Curtis, California’Department of Fish and a complex sequenceof stereotypedbehaviors that Game; K. Giesen, T. Remington,Colorado Depart- ment of Natural Resources:S. Simnson.Illinois De- includes tail fanning, erection of specializedneck partment of Conservation. R. Westemeier, Illinois , and vocalizations produced by brightly Natural History Survey; K. Church, Kansas Depart- colored inflatable air sacs(Sharpe 1968, Hjorth ment of Wildlife and Parks: W. Benz. Minnesota De- 1970). Centrocercusand Tympanuchus are not partment of Natural Resources;D. &dress, Montana closely related genetically and are partitioned into Department ofFish, Wildlife, and Parks;W. Vodehnal, Nebraska Game and Parks Commission; D. Burke, W. different groups by the molecular phylogeny. Collins, W. R. Skinner, Newfoundland Department of These observations suggestthat: (1) an “aggre- Culture, Recreation, and Youth; C. Roberts, Noble gative polygynous mating system” has evolved Foundation (Oklahoma); J. Kobriger, North Dakota SYSTEMATICS OF NORTH AMERICAN GROUSE 499

Department of Game and Fish; J. Mills, B. Sabean, DOWLING, T. E., C. MORITZ, AND J. D. PALMER. 1990. Nova Scotia Department ofLands and Forests; A. Cur- Nucleic acids II: restriction site analysis, p. 250- tie, J. Little, M. Twiss, Ontario Ministry of Natural 3 17. In D. M. Hillis and C. Moritz [eds.], Molec- Resources; L. Lang, Pennsylvania Game Commission; ular systematics. Sinauer Assoc., Sunderland, MA. G. Alain, Quebec Ministtre du Loisir, de la Chasse et ELLSWORTH,D. L., R. L. HONEXXJ~~, N. J. SILW, K. de la P&he; L. Frederickson, South Dakota Depart- D. RIT~NHOUSE, AND M. H. SMITH. 1994. Mi- ment ofGame, Fish, and Parks; J. Roseberry, Southern tochondrial-DNA and nuclear-gene differentia- Illinois University; H. Parker, Svaney Foundation; E. tion in North American prairie grouse (genus Follmann, University of Alaska; R. Baydack, Univer- Tympanuchus). Auk 111:661-671. sity of Manitoba; J. F. Bendell, University of Toronto; FELSENSTEIN,J. 1989. PHYLIP: phylogeny inference J. Teer, Welder Wildlife Foundation; R. Dumke, Wis- package (version 3.2). Cladistics 5: 164-166. consin Department ofNatural Resources; J. Derr, Tex- FITCH, W. M., AND E. MARGOLIASH. 1967. Construc- as A&M University, and F. Zwickel. tion of phylogenetic trees. Science 155~279-284. D. Ransom urovided valuable comments. K. Rit- FJELDSA,J. 1977. Guide to the young of European tenhouse and C. E&rich assisted in the Wildlife Ge- precocial birds. Skarv Nature Publications, netics Laboratory. This research was supported by grants Strandgarden, DK. 3220 Tisvildeleje, Denmark. from the National Science Foundation (BSR-9016327 GILL. F. B.. AND B. SLIM. 1992. Patterns of mito- to D. L. Ellsworth and BSR-8918445 to R. L. Honey- chondhal DNA divergence in North American cutt), the Welder Wildlife Foundation (contribution crested titmice. Condor 94:20-28. #443), and the American Ornithologists ’ Union (Al- GRANGE, W. 1940. A comparison of the displays and exander Wetmore fund). The senior author was par- vocal performances of the Greater Prairie-Chick- tially supported by a Graduate Deans ’ Merit Fellow- en, Lesser Prairie-Chicken, Sharp-tailed Grouse, ship and a Thomas Baker Slick Senior Graduate Re- and . Passenger Pigeon 2: 127-l 33. search Fellowship from Texas A&M University. HAMERSTROM, F. N., JR., AND F. HAMERSTROM. 1973. The prairie chicken in Wisconsin: highlights of a twenty-two-year study ofcounts, behavior, move- LITERATURE CITED ments, turnover, and habitat. Wisconsin Dept. Nat. Res. Tech. Bull. 64. ALDRICH, J. W. 1963. Geographic orientation of HJORTH, I. 1970. Reproductive behavior in Tetra- American Tetraonidae. J. Wildl. Manage. 27:529- onidae, with special reference to males. Viltrevy 545. 7: 184-596. AMERICAN ORNITHOLOGISTS ’ UNION. 1983. Checklist H~~HN, E. 0. 1980. Die Schneehtihner, 2nd ed. Neue of North American birds. 6th ed. Allen Press. Brehm-Bucherei, no. 408. A. Ziemsen Verlag, Lawrence, KS. Wittenbera Lutherstadt. AVISE. J. C.. AND W. S. NELSON. 1989. Molecular HOLMAN, J. A.-1964. Osteology ofgallinaceous birds. genetic relationships of the extinct Dusky Seaside Ouart. J. Fla. Acad. Sci. 27:230-252. Sparrow. Science 243:646-648. JOHA&EN, H. 1956. Revision und entstehung der AVISE, J. C., AND R. M. ZONK. 1988. Molecular genetic arktischen vdgelfauna. Acta Arctica 8: l-98.- divergence between avian sibling species: King and JOHNSGARD.P. A. 1973. Grouse and quails of North Clapper Rails, Long-billed and Short-billed Dow- America. Univ. of Nebraska Press: Lincoln, NE. itchers. Boat-tailed and Great-tailed Grackles. and JOHNSOARD, P. A. 1983. The grouse of the world. Tuftedand’ Black-crested Titmice. Auk 1055 16- Univ. of Nebraska Press, Lincoln, NE. 528. JOHNSGARD, P. A. 1994. Arena birds. Smithsonian BALLARD, W. B., AND R. J. ROBEL. 1974. Reproduc- Inst. Press, , DC. tive importance ofdominant male Greater Prairie- JOHNSTON, R. F., AND R. K. SELANDER. 1964. House Chickens. Auk 91:75-85. Sparrows: rapid evolution of races in North Amer- BEER, J. 1943. Food habits of the Blue Grouse. J. ica. Science 144:548-550. Wildl. Manage. 7:3244. JONES, R. E. 1964. The specific distinctness of the BLACKFORD,J. L. 1963. Further observations on the Greater and Lesser Prairie-Chickens. Auk 81:65- breeding behavior of a Blue Grouse population in 73. Montana. Condor 60:485-5 13. IOSSLER, L. G., AND J. C. AVISE. 1984. Systematic BRAUN, C. E. 1969. Population dynamics, habitat, relationships among waterfowl () inferred and movements of White-tailed Ptarmigan in Col- from restriction endonuclease analysis of mito- orado. Ph.D.diss., Colorado State Univ., Fort Col- chondrial DNA. Svst. Zool. 33:370-380. lins, CO. BRODKORB, P. 1964. Catalogue of fossil birds. Part 2 KESSLER,L. G., AND J. C. AVISE. 1985. A comparative ( through ). Bull. Fla. State description of mitochondrial DNA differentiation Mus. 8:195-335. in selected avian and other vertebrate genera. Mol. CARR, S. M., AND 0. M. GIUFF~TH. 1987. Rapid iso- Biol. Evol. 2:109-125. lation of mitochondrial DNA in a small LUMSDEN, H. G. 1968. The displays of the Sage fixed-angle rotor at ultrahigh speed. Biochem. Grouse. Ontario Dept. Lands and Forests Res. Genet. 25:385-390. Report (Wildlife) No. 83. CAVALLI-SFORZA, L. L., AND A.W.F. EDWARDS. 1967. MACDONALD, S. D. 1968. The courtship and terri- Phylogenetic analysis: models and estimation pro- torial behavior of Franklins’ race of the Spruce cedures. Evolution 21:550-570. Grouse. Living 714-25. 500 D. L. ELLSWORTH, R. L. HONEYCUTT AND N. J. SILVY

MACK, A. L., F. B. GILL, R. COLBURN,AND C. SFQLSKY. method: a new method for reconstructingphylo- 1986. Mitochondrial DNA: a source of genetic genetic trees. Mol. Biol. Evol. 4:406-425. markers for studies of similar passerinebird spe- SHARPE,R. S. 1968. The evolutionary relationships cies. Auk 103:676-68 1. and comparative behavior of prairie chickens. NEI, M., AND W.-H. LI. 1979. Mathematical model Ph.D.diss., Univ. of Nebraska, Lincoln, NE. for studying genetic variation in terms of restric- SHIELDS,G. F., AND K. M. HELM-BYCHOWSKI.1988. tion endonucleases.Proc. Natl. Acad. Sci. USA Mitochondrial DNA of birds, p. 273-295. Zn R. 765269-5273. F. Johnston [ed.], Current . Volume 5. ORING, L. W. 1982. Avian mating systems,p. l-92. Plenum Press, New York. In D. S. Famer, J. R. King, and K. C. Parkes[eds.], SHORT,L. L., JR. 1967. A review of the genera of Avian biology. Volume 6. Academic Press, New grouse(Aves, Tetraoninae). Amer. Mus. Novitates York. 2289: l-39. OVENDEN,J. R., A. G. MACKINLAY, AND R. H. CROZIER. SIBLEY,C. G., ANDJ. E. AHLQUIST. 1990. Phylogeny 1987. Systematics and mitochondrial genome and classificationof birds. Yale Univ. Press,New evolution of Australian rosellas (Aves: Platycer- Haven, CT. cidae). Mol. Biol. Evol. 4526-543. UPHOLT,W. B. 1977. Estimation of DNA sequence PETERS,J. L. 1934. Check-list of the birds of the divergence from comparison of restriction endo- world. Volume 2. Harvard Univ. Press, Cam- nucleasedigests. Nucleic Acids Res. 4: 1257-1265. bridge, MA. WETMORE,A. 1960. A classificationfor the birds of POTAPOV.R. L. 1985. Fauna of the USSR: birds. the world. Smithsonian Misc. Coll. 139:l-37. Volume 3. Order Galliformes, Family Tetraoni- ZINK, R. M. 1991. The geographyof mitochondrial dae. Science Institute, Leningrad (in Russian). DNA variation in two sympatric sparrows. Evo- RIDGWAY, R., AND H. FRIEDMANN. 1946. The birds lution 45:329-339. of North and Middle America. U.S. Natl. Mus. ZINK, R. M., AND D. L. DIITMANN. 1991. Evolution Bull., No. 50, pt. 10. of Brown Towhees:mitochondrial DNA evidence. SAITOU,N., ANDM. NEI. 1987. The neighbor-joining Condor 93:98-105.

APPENDIX 1. Locality data for North American grouseand ptarmigan specimensused in this study.

Ruffed Grouse (Bonusa umbellus)(ALASKA; North Star Borough, n = 1; MONTANA, FergusCo., n = 1; ONTARIO, CANADA, Ignace Municipality, n = 1; PENNSYLVANIA, Erie Co., n = 1; QUEBEC, CAN- ADA, Duplessis Comte, n = 1; WISCONSIN; Langlade Co., n = 1). SageGrouse (Centrocercusurophusiunus) (CALIFORNIA, LassenCo., n = 2; COLORADO; Gunnison Co., n = 1; JacksonCo., n = 1; SaquacheCo., n = 1; IDAHO, Clark Co., n = 1). Spruce Grouse (Dendrugupuscunudensis) (ALASKA; vicinity of Anchorage, n = 1; MANITOBA, CANADA, Grand Rapids Municipality, n = 2; NOVA SCOTIA, CANADA, Victoria Municipality, n = 1; ONTARIO, CANADA, Ignace Municipality, n = 1; QUEBEC, CANADA, SaguenayCorn& n = 1). Blue Grouse (Dendrugupusobscuncs) (COLORADO, Gunnison Co., n = 1; Routt Co., n = 1; MONTANA; Fergus Co., n = 1; BRITISH COLUMBIA, CANADA; Vancouver Island, n = 1). Willow Ptarmigan (Lugopuslugopus) (MANITOBA, CANADA, Leaf Rapids Municipality, n = 2; NEW- FOUNDLAND, CANADA, n = 2; QUEBEC, CANADA, Ungava Comte, n = 2; YUKON TERRITORY, CANADA, 299 km S Eagle Plains, n = 1). White-tailed Ptarmigan (Lugopusleucurus) (ALASKA, vicinity of Paxson, n = 2; COLORADO, Larimer Co., n = 2). Rock Ptarmigan (Lugopusmutus) (ALASKA; vicinity of Fairbanks, n = 1; NEWFOUNDLAND, CANADA, n = 1; QUEBEC, CANADA; Ungava Comtt, n = 1). Greater Prairie-Chicken (Tympanuchuscupido) (ILLINOIS: Marion Co., n = 1; KANSAS; Butler Co., n = 1; Shawnee Co., n = 1; NEBRASKA, Thomas Co., n = 1; OKLAHOMA, OsageCo., n = 1; SOUTH DAKO- TA, Lyman Co., n = 1). Lesser Prairie-Chicken (Tympunuchuspallidicinctus) (KANSAS; Clark Co., n = 3; Morton Co., n = 2). Sharp-tailed Grouse (Tympunuchusphusiunellus) (COLORADO; Routt Co., n = 1; MANITOBA, CANADA; Coldwell Municipality, n = 1; MINNESOTA, Aitkin Co., n = 1; NEBRASKA, Thomas Co., n = 1; NORTH DAKOTA, Billings Co., n = 1; QUEBEC, CANADA, Ungava Comtt, n = 1; SOUTH DAKO- TA; Lyman Co., n = 1). Capercaillie (Tetruo urogullus)(NORWAY, captive flock, n = 1). Northern Bobwhite (Colinus virginianus)(ILLINOIS; Williamson Co., n = 1).