The Auk 117(3):578-585, 2000
A PHENOTYPIC
TEST OF HALDANE'S
HYBRID
ZONE
CATHERINE
RULE
IN AN
AVIAN
E. SMITH 1 AND SIEVERT ROHWER
BurkeMuseumandDepartment
of Zoology,Box353010,Universityof Washington,
Seattle,
Washington
98195, USA
ABSTRACT.--We
introducea phenotypicmethodto testfor excessmortalityin hybridsof
the heterogametic
sex,as expectedfrom Haldane'srule, and apply this methodto the unusuallynarrow hybrid zonesbetweenHermit Warblers(Dendroica
occidentalis)
and Townsend'sWarblers(D. townsendi)
in the PacificNorthwest.Our testrequiresestablishing
comparablehybridindicesfor male and femalewarblers.The hybrid indexthat we developed
for femalesproducedage-corrected
distributionsfor phenotypicallypurereferencesamples
that closelymatchedthoseusedby Rohwerand Wood (1998)for males.The similarityin
thesedistributionsenabledus to comparethe relativefrequencyof malesand femalesin
hybridsandparentals.Wedetectedno deficiency
of hybridfemalesandthusno inviability
in the heterogametic
sex.Our failure to find evidenceof the inviabilitycomponentof Haldane'srule is not unexpectedgiventhe closerelationshipbetweenthesetaxa;nonetheless,
ourmethodsshouldbe generallyusefulfor studiesof hybridzones.Received
7 December
1998,
accepted
2 October1999.
HERMIT (DENDROICA
OCCIDENTALIS)
and Town- are narrow relative to root mean square dissend's(D. townsendi)
warblersdivergedduring persal are characterized
by hybrid inferiority
the middle Pleistocene,
presumablyin coastal relative to parentals(Bartonand Hewitt 1985,
(Hermit) and RockyMountain (Townsend's)re- 1989).Here, we examinea component
of this
fugia (Berminghamet al. 1992).Both species possibility by exploring the applicabilityof
nestand foragein the canopiesof tall conifers Haldane'srule to thesewarblerhybrid zones.
in the PacificNorthwest.Today,their ranges Reduced fertility and reduced viability in
meet at threenarrowhybrid zones:the Olym- hybridsoften are expressedin the heterogapic Mountains of Washington,the southern meticsex,a phenomenon
first notedby J.B. S.
Cascadesof Washington,and the Cascadesof Haldane in 1922 and now known as "Haldane's
Oregon south of Mount Hood (Rohwer and rule." Recentworkhasgenerateda strongconWood 1998).Two well-describedhybrid zones sensus
regardingthecausalmechanism
underin Washingtonare slightlymore than 100 km lying Haldane'srule: alleles causinghybrid
wide, making them only three to four times problems("speciationgenes")actaspartialrewider than estimatesof the root meansquare cessives,leading to preferentialexpressionof
dispersaldistance(31 km; Rohwerand Wood deleteriousrecessives
in hybridsof thehetero1998).Thenarrowness
of thesezonessuggests gametic sex (Turelli and Orr 1995, Orr 1997).
that some sort of balance between selection and
Thesepartial recessives,
or speciationgenes,
are
expressed
in
hybrid
offspring
whenthegewider (Rohwer and Wood 1998, Barton and
nomes
of
isolated
lineages
recombine
through
Gale 1993).
the
initiation
of
hybridization
during
secondConsiderableevidencesuggeststhat these
ary
contact.
As
long
as
"speciation
genes"
act,
zonesremainnarrowbecause
hybridsarecomdispersalis preventingthem from becoming
petitivelyinferiorto Townsend's
Warblers,and,
further,thatthesezonesaremovingsouthward
becauseTownsend'sWarblersand hybridsare
competitively superior to Hermit Warblers
(Rohwer and Wood, 1998, Pearson2000, Pearsonand Rohwer2000).Mosthybridzonesthat
E-mail:[email protected]
578
on average,as partial recessivesin genomesof
mixed ancestry,hybridsof the heterogametic
sexwill tend to fare worsethan hybridsof the
homogametic
sex.
Haldane'srule appearsto be a very important mechanism
for speciation,
with sterilityor
inviabilityof hybridsof the heterogametic
sex
characterizingspeciationin a wide variety of
animals(e.g.Grula and Taylor1980,Coyneand
July2000]
Warbler
HybridsandHaldane's
Rule
579
Orr 1989,Virdee and Hewitt 1992).Using com- from the hybrid zonesbetween20 May and 31 July
parative data on hybridizationin Drosophila, were used as referencesamplesto assessthe range
Coyneand Orr (1989)showthat sterilityor in- of phenotypicvariationin parentals.For Hermit
Warblers, reference females were collected from the
viability in hybrid males (the heterogametic
southwesternCascadesof Oregonand from Califorsex)may representan early stagein speciation. nia. For Townsend's Warblers, reference females
Althoughresearchon Haldane'srule hasbeen werecollectedin regionsto thenorthandwestof the
largelyrestrictedto speciesthat canbe bred in hybrid zones.
captivity,field studieson hybridizingflycatch- Agedetermination
infemales.--Townsend's
Warblers
ers (Ficedulaalbicollisand F.hypoleuca)
revealed of both sexesare more boldly marked than Hermit
no exchangeof mitochondrialgenesthrough Warblers, and adult birds of both sexes are more
hybridfemales(theheterogametic
sexin birds) boldly markedthan yearlings.Forthis reason,yearbut dramatic evidence of interspecificflow of
ling Hermitsandhybridson averagehavelowerhy-
reliablydisnucleargenesthroughhybrid males (Tegel- brid indicesthan adults.Consequently,
criminatingyearlingandadultfemalesis essentialto
combiningtheirscores
withoutintroducingvariance
relatedto agedifferences
ratherthanto hybridparentage.Becauseour objectivewas to developaging
(Gelter et al. 1990).
criteria applicableboth to hybrids and parentals,
Despitethe relativelycommonoccurrence
of known-agebirdsof bothspecieswerepooledfor the
interspecifichybridizationin birds (roughly developmentof agingcriteria.
Referencespecimensfor aging included autumn
10%of speciesare knownto hybridize;Grant
str6m and Gelter 1990). In accordancewith
Haldane'srule, hybrid femaleswere shownto
be infertile, whereashybrid males were not
and Grant 1992), avian field studies that addresshybrid inferiority are rare, and hybridizationis still studiedlargelythroughmorphological analysesof collectedspecimens.Here,
females with data on skull ossification; females with
we developa morphologicalapproachto explore the applicabilityof Haldane'srule to
studiesof hybrid zones.Becausefemalebirds
are heterogametic,hybrid femalesshouldbe
samplebecauseyoungbirds do not molt their primariesin the year they are born (Jackson
et al. 1992,
Pyle 1997). Heterogeneityin our initial reference
sampleforcedus to reassessa numberof specimens.
We eliminatedeight late-summerbirds labeled as
immaturesbut clearlyin adult plumage(with the
distinctmarkingsthat yearlingslack).We alsoeliminated four late-autumn birds with fully ossified
skullsbut in immatureplumage,becauseyearlings
may have completelyossifiedskulls by this time
(Pyle 1997).With this modifiedreferencesampleof
known-agebirds, we identifiedtraits that reliably
predictedage and appliedthesecriteriato spring
and summerbirds of unknown age.
Plumagecharacteristics
that distinguishthe age
classesof malesalso may distinguishthoseof females.Adult malesof bothspecieshavemorewhite
on their fourth rectricesthan do yearlings(Jackson
et al. 1992).In addition, yearling malestend to have
thick,black,v-shapedstreakson the shaftsof their
medial secondarycoverts,whereasadult maleshave
more linear, narrow streaks(Jacksonet al. 1992,Pyle
more prone to decreasedfertility and survivorship than hybrid males(Haldane1922,Coyne
and Orr 1989). To comparemales and females,
we developa hybrid index for female Hermit
and Townsend'swarblers and their hybrids
that closelymatchesthe index developedby
Rohwer and Wood (1998) for males. If female
hybrids are sufferingexcessmortality,there
shouldbe a shortageof femalehybridsrelative
to male hybrids for phenotypesmidway betweenthe parentals.Shouldthis predictionbe
upheld, "speciationgenes"generatinginferiority of hybridsto both parentalsmight help
explainthe narrowness
of thehybridzonesbetween Hermit
and Townsend's
warblers.
METHODS
We examined284 museumspecimensof female
Townsend'sWarblersand Hermit Warblersand part
of the malesampleemployedby Rohwerand Wood
(1998).Femalescollectedbetween1 August and 31
December,
with ageinformationontheirlabels,were
usedto developcriteriafor distinguishing
birdsin
their first year of life (i.e. yearlings)and older females (i.e. adults). Femalescollectedat least 250 km
remnantsof juvenal plumage;and femaleslabeled
adult, immature, or juvenile by the collector.One
late-summerfemale (AMNH89672) with sheathing
on the base of P9 was included
in the adult reference
1997). We assessedthese charactersfor all known-
agefemalesby measuringthe white spoton the left
and right fourthrectrices(greatestlengthx greatest
width, in mm2) and then averagingthe two measurements,and by notingthe type of streakingon
the shaftsof the medialsecondarycoverts.
Our sampleof known-agefemalesconsistedof 10
adultsand85 yearlings.Thedistributionof tail-spot
sizeswasdistinctlybimodal;the averagesizeof the
tail spotsof all but one adult was greaterthan 25
580
SMITHANDROHWER
Adults
n=10
0
10
I ,.,.
20
40
50
60
110
60
Yearlings
50
n= 85
ß
40
30
• 20
10
0i ' [ ' [f [ ' ] ' i ' [ ' • '
0
10
20
30
40
50
60
70
80
Area(mm2)of fourthrectrixspot
FIG. 1. Frequencydistributionof tail-spot sizefor
known-agewarblers.Arrows at 25 mm2indicatethe
division used to separatefemalesof unknown age.
mm2,and the tail spotsof all but two yearlingswere
lessthan 25 mm• (Fig. 1). Using 25 mm• as the division,the ageof 92 of 95 birds (97%)wasdetermined
correctlybasedon the size of their tail spots.In addition, 78 of 94 birds (83%) were correctly aged by
shaft streaking:9 of 10 adults had narrow shaft
streaking and 69 of 84 yearlingshad thick shaft
streaking.We used tail-spot size as our primary aging criterion,but we used shaft streakingto determine the ageof 10 breedingbirdsthat weremissing
both of their fourth rectrices.
Characterscoring.--FollowingRohwer and Wood
(1998), we quantifiedcolor characterswith numeric
scores,using 0 for the most Hermit-like statesand
higher values for the most Townsend's-likestates
(Table1). Sixof the sevencharacters
usedby Rohwer
and Wood (1998) for males could be applied to females;"bib corner"couldnot be usedbecausemany
yearling femalesdo not have bibs. We assignedas
many units as we could reliably distinguishto the
remaining six characters(Table 1). Scoresfor each
characterwere standardizedto vary from 0 to 1 to
equalizeweighting.To facilitatefuture work, all of
the referencespecimensused to define character
states(Table1) are from the Universityof Washington Burke Museum (UWBM).
Character
descriptions.--We
scoredflank streaking
for the mid and the lower flanks, becausethese char-
o y
[Auk,Vol. 117
July2000]
Warbler
Hybrids
andHaldane's
Rule
10
Adults
10
Adults
8
n = 22
8
n = 22
6
.•
58]
6
....
o
0
o
10
20
30
0.0
.,.,.,.,....,
0.4
0.8
1.2
1.6
o
20
Yearlings
20
Yearlings
16
n = 39
16
n = 39
12
12
0
....
0
, ......
10
,•. •
20
30
Extentof Yellow
0
. , , , . , , , , , .
0.0
0.4
0.8
1.2
.
, ,
1.6
LogExtentof Yellow
F•c. 2. Frequencydistributionsof the character"extent of yellow" (mm) for femalereferenceadults
(above)and yearlings(below)before(left) and after (right) log transformation.
actersappear to be under independentgeneticcontrol (Rohwer and Wood 1998). The flanks are often
washedwith a buffy tinge in yearling females;the
streaks,if present, are gray, but often are indistinct
in Hermits and hybrids. Buffinesswas ignored in
scoringflank streaking,and the gray streakingwas
scored.Extentof yellowon the breastwasmeasured
in mm from the posterioredgeof the"shadow"correspondingto thebib typicallyfoundon adultmales
to the posterioredge of the yellow feathering.The
shadowwasapparenton virtually all specimens;
for
the few problematicyearlings,the posterioredgeof
the shadowwas approximated.Intensityof yellow
on the breastwas scoredfrom no yellow to very intense.Extent of yellow on the breast,measuredin
mm, is so highly variablein femalesthat we transformed thesescoresto logs to make their distributionscomparableto the other characters(Fig. 2). To
make these transformed scores start at 0, we added
1 prior to convertingscoresto logs.Withoutthis log
transformation,the final hybrid index for the Townsend's reference females would be skewed to the left
(left half of Fig. 2), makingthe femaleindexincomparableto that for males.Extent of yellow on the
crown is highly variablein hybridsbut difficult to
scorebecauseHermitsand hybridsoftenhavegreen
rather than yellow crowns. The head feathersof
Townsend'sWarblersare entirely gray or blackfrom
base to tip. We quantified crown color variation by
gentlylifting the headfeathersand scoringthe yel-
low colorationof their midshaftregion.We scored
backcolor(but not backstreaking)emphasizingthe
rump, where streakingis reduced.
Standardizing
scores
andthehybridindex.--Toeliminate age-related variation, we corrected for mean
differencesbetweenageclasses
by standardizingthe
scoresfor adults and yearlingsseparately.For several characters,
a few yearlingsreceivedfully adult
scores. To better match the reference distributions
for
the two age classes,we assignedthe next mostfrequentscoreto thosefewyearlingsthatwereasboldly
markedas adults.By dividingby the maximumvalue assignedto eachagegroup,scoresfor eachcharacter were scaledto vary from 0 (Hermit extreme) to
1 (Townsend'sextreme).The sum of thesesix stan-
dardized characterscoreswas then divided by 6 to
generatethe final hybridindexfor females,hereafter
Sum6st,that was comparableto Sum7stfor males
(seeRohwer and Wood 1998).
Specimen
localities.--Phenotypic
testsof Haldane's
rule apply only to birds of hybrid origin. For phenotypiccomparisonof the sexes,we used only hybrid localities, defined as localities with
mean
Sum7stfor malesbetween0.2 and 0.8 (Rohwer and
Wood 1998).We used mean locality scoresfor males
to identify hybrid localitiesbecausefemalesof these
treetop warblersare rarely collected.Becauseno femaleswerecollectedat manyof the localities,we includedmalesfrom a localityonly if we alsohad femalesfrom that locality.
582
SMITHANDROHWER
[Auk,Vol. 117
35
Forourphenotypictestof Haldane'srule,theideal
hybrid samplewould containmany males and femalesand would havebeentakenat the phenotypic
centerof the hybrid zone.In narrow hybrid zones,
suchlocalitiesmaycontainsubstantialnumbersof F•
hybrids,to whichHaldane'srule is mostapplicable.
•
The shortageof femalespecimens
of thesewarblers
precludedrestrictingour samplingto midpoint localities.Althoughthis is lessthan ideal, the narrownessof their zonesrelativeto root meansquaredispersal distancesuggeststhat mosthybrid localities
couldcontainF• hybrids.Furthermore,the "specia-
Males
n = 122
30
25
20
15
10
5
'
0
'
'
I
'
0.2
I
0.4
tion genes" responsiblefor Haldane'srule can also
be expressedin non-F•hybrids.
Analysis.--If Haldane'srule is operating,we would
expecta deficiencyof hybridsof the heterogametic
sex (femalesin birds), which would be detectedas a
12
Females
deficiencyof hybrid females,especiallyof pheno-
10
n =61
,
i
,
i
,
0.6
i
,
,
,
0.8
1.0
0.8
1.0
$um7st
types midway between parentals.To test for a defi-
ciencyof mid-phenotypefemales,we comparedthe
frequencyof parentalsand hybridsfor females(using Sum6st)with thosefor males(usingSum7st).For
this analysis, both distributions of standardized
scoreswere divided into thirds. Birds scoring0 to
.•
8
=
6
4
2
0.333 were pure Hermits and Hermit-like backcross-
es;thosescoring0.333to 0.667weremid-phenotype
hybrids;and thosescoring0.667to 1.000were pure
Townsend's
and
Townsend's-like
backcrosses.
Be-
causeHaldane'srule contrastshybridswith parentals,birdswith phenotypicscoresfrom 0.333to 0.667
were treatedashybrids,and the two extremeparental classeswere pooled.
'
0
ß
0.2
' i , i ' i ' i ....
0.4
Sum6st
FIG. 3. Frequencydistribution of hybrid index
scoresfor reference males (above) and females (be-
low). Note that the "phenotypicspace"between
Sum6st scores for reference
RESULTS
0.6
females matches that of
Sum7stscoresfor referencemalesand is similarlybimodal.
Can male and female hybrid indicesbe compared?--For the phenotypic comparison of
malesand females,the hybrid indicesfor sam- indices could be treated as equivalentin our
plesof both sexescollectedwell outsidethehy- phenotypictestof Haldane'srule.
brid zonesmust have matchingdistributions. Testingfor HaldaneSrule.--Acrossthe three
Moreover,the phenotypicspaceseparatingthe classes
of phenotypes,
thefrequencyof females
referencesamplesof the two species(wherehy- nearlymirroredthat of males,offeringno sugbrids should fall) must be of similar size for gestionof female inviability in thesewarbler
malesand females.Evaluatingthis is a critical hybrids(Fig. 4). Our samplescontainedmore
issue becauseour hybrid index for females Hermit and Hermit-like hybridsof both sexes,
(Sum6st)containedfewer charactersand fewer but thismerelyreflectedthegreatergeographic
character
states than
did that for males
spacecoveredby the Hermit sideof thesezones
(Sum7st).
(Rohwer and Wood 1998).
Phenotypicvariation within males and feAlthoughFigure4 dividesphenotypicspace
maleswas remarkablysimilar (Fig. 3), leaving into threeregions,we pooledthe two classes
of
a similar gap for hybrid phenotypes.All Her- parentalsand parental-likebackcrosses
in our
mit reference females had scores of less than
testfor a deficiencyof hybrid females(Table2).
0.2, and all but three Townsend's reference fe- Combiningtheseclassesto make this a 2 x 2
maleshadscores
greaterthan0.8(Fig.3).Thus, testfor hybridinviabilityin the heterogametic
Sum6stfor femaleswas comparableto Sum7st sexis importantbecausethe three-groupanalfor males,andthesesomewhatdifferenthybrid ysissuggested
by Figure4 couldbe significant,
July2000]
WarblerHybridsandHaldane's
Rule
Males
n = 191
8O
60
40
TABLE2. Two-by-twotableof male and femalewarbiersfrom hybridlocalitiesdividedinto "parental
and parental-likebackcrosses"(hybrid index 0 to
0.333and 0.667to 1.0) and "hybrids" (hybridindex 0.333 to 0.667) as describedin Methods.
Phenotype
Parental
Hybrid
20
583
Males
Females
131 (69%)
60 (31%)
20 (74%)
7 (26%)
0
0
0.33
0.67
1.0
can be usedto evaluatethe inviability compo-
Sum7st
nent of Haldane's
14
Females
12 •
n=27
10
rule.
The similarlylargephenotypicgap separating parentalphenotypesof malesand females
in thesewarblerssuggests
that hybridsshould
be equallydetectablein both sexes(Fig.3). We
cautionthat the similar distributionsof phenotypic scoresfor males and femalescould reflectthe similarpatternof the colorationof the
two sexes in these warblers.
4
Because most of
our characters could be scored for both sexes,
2
0
0
0.33
0.67
1.0
Sum6st
they are likely controlledby largely overlapping sets of genes.Although this lends credenceto our comparisonsof male and female
phenotypesin these warblers,such comparisonsmay not be possiblefor hybridizing taxa
FzG.4. Frequencydistribution of hybrid male in which females do not resemble males.
(above)and female(below)scoreswhen phenotypic
Our phenotypicanalysesfailed to detect a
spaceis divided into thirds(0 to 0.333,0.333to 0.667, shortageof femalehybrids(Fig. 4, Table2), in0.667 to 1.0).
withoutsupportingHaldane'srule.Thiswould
happenif femalesof oneparentalspecieswere
easier to collect, relative to males, than females
of the other parental species.The 2 x 2 test
showedno evidenceof a deficiencyof hybrid
femalesin samplescollectedfrom hybrid localities (Fisher'sexacttest, P = 0.66; Table 2).
DISCUSSION
Our researchmakestwo importantcontributionsto the studyof hybrid zones.First,we
presentdata showingthat the separatehybrid
indices used for males and females in these sex-
ually dichromaticwarblershavesimilardistributions(Fig. 3). The similarity of thesedistributionsmakesit possibleto pool malesand femalesof sexuallydimorphicspeciesin studies
of hybrid zones.Second,we showhow comparisonsof hybrid indicesfor males and females in samplesof field-collectedspecimens
dicatingthat viability of midpoint phenotypes
is no less in females(the heterogameticsex)
than in males.This suggeststhat male and female hybrids survive equally well. Haldane's
rule may alsobe expressedby reducedfertility
in hybrids,whichcannotbe addressedphenotypically. Pearsonand Rohwer (1998) examined onecomponentof reducedfertility in hybridsby comparingclutchsizesof hybridswith
thoseof parentalsfrom areasnear the hybrid
zones. Clutchesof hybrids were smaller than
thoseof both parentalsand were significantly
smallerthan thoseof pure Townsend's,
the parental speciesthat lays the largest clutches
(Pearsonand Rohwer 1998).
Our failure to detect female inviability further supports the notion that competitive
asymmetriesaccountfor the narrownessof the
hybrid zones.If hybrids are inferior to one of
the parentals,selectionshouldkeep the zones
narrow. Character-transitionanalysesindicate
that more Townsend'sgenescrossthe zones
into Hermit populationsthan vice versa,suggestingthat the zonesaremoving(Rohwerand
584
SMITH
ANDROHWER
Wood 1998).Within hybrid zones,male Townsend'saremoresuccessful
atholdingterritories
and attractingfemalesthan are male Hermits
and hybrids(Pearson2000). This is probably
due to differencesin aggressiveness;
Townsend's males are more aggressive toward
mountsof both parentalphenotypesthan are
Hermit males (Pearsonand Rohwer 2000). Unlike the casein manynarrowzoneswherehybrids are less fit than parentals(Barton and
Hewitt 1989),hybrid malesare more aggressivethanpureHermitsbut lessaggressive
than
pure Townsend's.Our failure to detect inviability in femalehybridsaddsto a growingbody
of information suggesting that behavioral
asymmetries between parental species are
largelyresponsible
for the apparentsouthward
movementof the zonesand that the competitive inferiority of hybrids to parental Townsend'sis responsiblefor the narrownessof the
[Auk,Vol. 117
are far removed from current hybrid zones
(Rohwerand Wood 1998).
Although Coyne and Orr (1989) use Nei's
(1987)geneticdistance(D; whichcannotbe di-
rectlycompared
with dxy)to indexdivergence
time, the patternthey detectedshouldbe applicable to other taxa. Becauseof the limited
time sincedivergence,
hybridsbetweenclosely
relatedspeciesareunlikelyto be detrimentally
affectedby "speciationgenes,"whichare deleteriousrecessivesexpressedonly in individuals of hybrid ancestry.Thus, Hermit and
Townsend'swarblersmay well be too closely
relatedto showinviabilityin hybridsof theheterogameticsex.Our analysesprovidedno evidenceof femaleinviabilityin thesewarblerhybrids, but we believe that the methods we de-
velopedfor examiningthis questionwill be
usefulin studiesof otherhybrid zones.
zones.
ACKNOWLEDGMENTS
Discussionsof Haldane'srule (see Orr 1997)
The specimensused for this work camefrom the
reveal that viability of hybridsin thesewarfollowing
institutions:AmericanMuseumof Natural
blers may be expected.Using the correlation
betweengeneticdistanceand divergencetime History (AMNH), California Academyof Sciences,
Charles R. Conner Museum, Delaware Museum of
in 119 speciesof Drosophila,Coyne and Orr
Natural History,Field Museumof Natural History,
(1989)showthatastaxadiverge,disadvantage LouisianaState University Museum of Natural Scito theheterogametic
sexis thefirstsymptomof ence,NaturalHistoryMuseumof LosAngelesCounhybrid malfunctionand, further,that sterility ty, SlaterMuseumof Natural History,UnitedStates
and viability disadvantages
are lesslikely in NationalMuseumof Natural History(USNM), Unihybridsbetweenrecentlydivergedtaxa. Be- versityof CaliforniaMuseumof VertebrateZoology
cause of their conduciveness
to laboratory (UCMVZ), Universityof Michigan Museumof Zostudy, breeding experimentswith Drosophila ology (UMMZ), Universityof NevadaBarrackMuBurkeMuform the only substantialbody of work from seum,and the Universityof Washington
which broadergeneralizations
can be drawn. seum(UWBM). SergeiDrovetski,Chris Filardi, and
No such comparativework is available for Gary Voelker commentedon earlier drafts of this
work, andScottPearsonhelpedwith all phasesof its
development.
JimRisingand an anonymous
reviewUsing mtDNA restriction-site data, Ber- er madehelpfulcommentson the manuscript.Garmingham et al. (1992) found a nucleotidese- rett Eddy hassupportedmostof the field work on
quence
divergence
value(dxy)
of0.0062between thesehybridzones.CESwassupportedby a NationTownsend'sand Hermit warblers,by far the al ScienceFoundationGraduateFellowshipand as a
smallestdivergencevalue for the five taxa ex- Burke Museum Eddy Fellow during this work.
birds.
amined
in this clade. This is also one of the
smallestestimatesof divergencebetweencongenericspeciespairs in birds (Berminghamet
al. 1992, Klicka and Zink 1997). Because
mtDNA is maternallyinherited,similaritiesbetweencloselyrelatedspeciescouldreflectpast
Thanks to all of these individuals
LITERATURE
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and institutions!
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from California
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