Phylogeny and Rates of Molecular Evolution in the Aphelocoma Jays (Corvidae)
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The Auk 109(1):133-147, 1992 PHYLOGENY AND RATES OF MOLECULAR EVOLUTION IN THE APHELOCOMA JAYS (CORVIDAE) A. TOWNSEND PETERSON• Committeeon Evolutionary Biology, University of Chicago,Chicago, Illinois 60637, USA ABSTRACT.--Iexamined hypotheses of Aphelocomajay phylogenyderived from allozyme data.Results from various algorithms differ in details,but the overallpatterns are consistent: ScrubJays (A. coerulescens)and UnicoloredJays (A. unicolor)were derivedindependently from differentpopulations of Gray-breastedJays (A. ultramarina).Within ScrubJays, the californicasubspecies group was derivedfrom the populationsof interior North America (woodhouseiigroup). One UnicoloredJay population and two ScrubJay populations, all strong- ly differentiated,are placedconsistently at the baseof the phylogeny,but phenotypic,bio- geographic,and theoreticalevidence suggests that thesepopulations represent rapidly evolv- ing populationsderived from within populationsof theirrespective species. Because analyses of ratesof molecularevolution demonstrate significant rate heterogeneity,I suggestthat the applicationof a molecularclock to date-splittingevents in the Aphelocomajays is not a valid approach.Received 18 February1991, accepted 3 July 1991. THE THREEspecies of Aphelocomajays range erra Madre Occidental);and (3) ultramarinagroup throughout western and southern North Amer- (TransvolcanicBelt). Finally, the UnicoloredJay ica and northern Central America (Fig. 1; Pi- (A. unicolor)consists of five allopatric popula- telka 1951). Scrub Jays (A. coerulescens)range tions, each a separatesubspecies, in southern from Oregon and Wyoming south to the Isth- Mexico and northern Central America (Pitelka musof Tehuantepec,with disjunctpopulations 1951). on Santa Cruz Island off the coast of southern The Aphelocomajays have been the subjectof California and in peninsular Florida. The 15 numerous comparativestudies. Evaluations of subspeciesform five groups,each characterized socialsystems in the genushave led to advances by unique combinationsof plumage, morpho- in understanding ecologicalfactors important logical, and behavioral characters(Fig. 1; Pi- in the evolution of sociality(Woolfenden and telka 1951,Peterson 1991a): (1) woodhouseiigroup Fitzpatrick 1984, Fitzpatrick and Woolfenden (Wyoming and southeastern Oregon south 1986,Brown 1987,Peterson and Burt, in press). through Great Basin and along both sides of Differential habitat use in ScrubJays (Peterson RockyMountains, and then alonginterior slopes and Vargas1992) is correlatedwith geographic of Sierra Madre Oriental and Sierra Madre Oc- variation in beak shape, suggestingthat beak cidental of northern Mexico to southern Chi- shapeshave respondedto natural selection(Pe- huahuan Desert and vicinity of Mexico City); terson, in prep.). Integration of phylogenetic (2) californicagroup (western Oregon, Califor- information into suchinvestigations will allow nia, and BajaCalifornia); (3) sumichrastigroup an important new dimensionof understanding (southern Mexico); (4) coerulescensgroup (pen- (Brooks and McLennan 1990). Hence, I have insular Florida); and (5) insularisgroup (Santa attemptedto estimatethe phylogeny of the dif- Cruz Island). The Gray-breastedJay (A. ultra- ferentiated forms in the genus. marina) ranges throughout the mountains of Ratesof molecularevolution.--Since the pub- northern and central Mexico and the south- lication of the influential paper of Zuckerkandl western United States.The sevensubspecies fall and Pauling (1962), the idea of a "molecular into three groupscharacterized by unique com- clock" has been controversial in molecular bi- binations of morphological and behavioral ologyand systematics.The clockconcept is based characters(Fig. 1;Pitelka 1951 ): (1) potosina group on the assumptionof a uniform rate of molec- (SierraMadre Oriental); (2) wollweberigroup (Si- ular evolution in a group. If the uniform rate assumptionwere correct, the accumulationof geneticdifferentiation between sister taxa would •Present address:Department of Zoology, Field be time-invariant, and divergence times could Museum of Natural History, RooseveltRoad at Lake be estimatedfrom genetic distances. Shore Drive, Chicago,Illinois 60605, USA. The clock conceptis an important feature of 133 134 A. TOWNSENDPETERSON [Auk, Vol. 109 many sectors of molecular systematics.At- tempts have been made to calibrate clocksfor a variety of taxa and biochemicaldata sets(e.g. Sarich 1977, Wilson et al. 1977, Sibley and Ahlquist 1981). Several commonly used tree- building algorithmsdepend on the assumption of a clock (Felsenstein 1982, 1989). The molec- ular clock is now a common method of dating divergencetimes between taxa (e.g. Zink 1982, Nevo et al. 1987, Johnson and Marten 1988). Hence, a uniform rate of molecular evolution and the consequentexistence of a clock can be important assumptionsin molecular systemat- ics. However, the assumption that evolutionary rates are homogeneousoften goes untested. If molecular evolutionary rates differ among lin- eages,the clockbecomes unreliable. Equality of rates in sister lineages can be tested with the relative-rate test: in the three-taxon statement ((A, B), C), A and B should show similar degrees of differentiation from C (Wilson et al. 1977). Significant departure from equality indicates that A and B have evolved at different rates. Rateuniformity hasbeen testedin a number of taxa, with some studies documenting homo- geneity (e.g. Sibley and Ahlquist 1983, Bledsoe 1987), and others finding heterogeneity (e.g. Britten 1986, Sibley et al. 1987, Sheldon 1987, Springerand Kirsch 1989).A uniform rate and molecularclock are commonlyand uncritically assumedin systematicstudies, so a test of the assumptionof rate uniformity was desirablein my study. METHODS Samplingdesign.--During 1986-1989, I studiedand collectedAphelocoma jays at 35 sites in the United Statesand Mexico.Tissue from the endangeredFlor- ida population of Scrub Jayswas salvagedfrom re- Fig. 1. Summaryof collectinglocalities and sub- cently dead individualsat nestsand roadsides.Sam- speciesgroups of three speciesof Aphelocomajays; ples of heart, liver, and pectoralmuscle from each Florida range indicatedin upper right-hand corner. individual were stored in cryotubesin liquid nitro- (A) ScrubJays: open circle, Santa Cruz Island(ACINS); gen. All tissuewas depositedin the Frozen Tissue closedcircles; californica group (CO CAL); closedtri- Collection of the Field Museum of Natural History. angles,northern woodhouseii group (CO WOO); open In total, I analyzed615 Aphelocomajays (458 Scrub triangles, southern woodhouseiigroup (CO MEX); Jays,138 Gray-breasted Jays, and 19 UnicoloredJays). squares, sumichrastigroup; dotted circle, Florida Specimensof Scrub,Gray-breasted, and Unicolored (ACCO2).(B) Gray-breasted Jays: triangles, wollweberi jayswere collectedat 24, 8, and 3 sites,respectively, group (UL WOL); circles,potosina group (UL POT); in the United Statesand Mexico (Table 1, Fig. 1). I squares,ultramarina group (UL ULT). (C) Unicolored attemptedto obtainsamples of 20 individualsat each Jays:triangles, east slope populations (UN E); circle, site to maximize tree stability (Archie et al. 1989): west slope population (ANGUE). ScrubJay samples averaged 19.2 (range 13-27) indi- viduals; Gray-breastedJay samplesaveraged 17.3 (range7-22) individuals;and UnicoloredJay samples January1992] Jay Phylogenyand EvolutionaryRates 135 TABLE1. Samplelocalities and samplesizes (complete locality data in Peterson1990). Sample Group Sample Locality size Scrub Jays CO CAL ACCAL CA, Monterey Co., Bradley 24 ACCAU CA, Trinity Co., Hyampom 16 ACHY3 BCS,Sierra de la Laguna 16 ACIMM OR, Adair Village 15 ACOBc CA, Orange Co., Silverado Canyon 16 ACOBk BCN, Rosade Castilla (Ojos Negros) 20 ACOOC CA, San Ramon 16 ACSP1 CA, Alturas 22 ACSP3 CA, Bodfish 19 CO MEX ACCY1 COA, E1 Diamante Pass 21 ACCY2 SLP, Sierra de Bledos 21 ACGR! DUR, Villa Ocampo 21 ACGR3 JAL, Lagosde Moreno 20 CO WOO ACNE! NV, Toiyabe Mountains 14 ACNE4 NV, Mt. Charleston 27 ACNE6 AZ, Drake 25 ACTEX TX, EdwardsPlateau, Carta Valley 22 ACWO! CO, Front Range,Gardner ! 1 ACWO3 NM, Manzano Mountains 26 ACWO4 TX, Davis Mountains 21 CO SUM ACREM GRO, Xocomanatl/•n 13 ACSM2 OAX, Sierra de los Mijes, Zempoalt•petl 20 ACINS CA, Santa Cruz Island 14 ACCO2 FL, Archbold Biol. Station 18 Gray-breastedJays UL WOL AUAZ1 AZ, Pefia Blanca Lake 16 AUGRA JAL, Sierra de Bolafios 7 AUWO1 ZAC, Valparaiso 20 UL POT AUCO2 COA, Sierra E1 Carmen 22 AUPO2 SLP, Sierra de Bledos 22 AUPO3 HID, Jacala 20 UL ULT AUULT MOR, Huitzilac 14 AUCOL JAL, Sayula 17 Unicolored Jays ANGUE GRO, Sierra de Atoyac 7 UN E ANOAX OAX, Sierra de los Mijes, Zempoalt•petl 10 ANCON HID, Sierra de la Huasteca, Tlanchinol 2 averaged6.3 (range2-10) individuals.To avoid prob- largerinfraspecific divisions, I dividedthe speciesin lemswith nonindependenceof individualgenotypes a manner equivalentto the subspeciesgroups of Pi- when relatedindividuals (e.g. parents and offspring, telka (1951),except that the woodhouseiigroup was multiplesiblings) were collected, I includedonly one dividedinto northern(United Statespopulations) and memberof each potentially related pair of individ- southern(Mexican populations)parts (Fig. I, Table uals. 1). For conveniencein referring to populationsam- To provide outgroupsfor phylogeneticanalyses, I ples, I assignedeach a five-letter code,in which the included70 individualsof 17 other corvidspecies. To first letter indicatesthe genus,the secondindicates maximizedetection of plesiomorphicalleles for po- the