Intraspecific Sympatry in a "Ring Species," the Plethodontid Salamander Ensatina

eschscholtzii, in Southern California

Author(s): David B. Wake, Kay P. Yanev and Charles W. Brown
Source: Evolution, Vol. 40, No. 4 (Jul., 1986), pp. 866-868
Published by: Society for the Study of Evolution
Stable URL: http://www.jstor.org/stable/2408473 .
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866 NOTES AND COMMENTS

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Evolution,40(4), 1986, pp. 866-868

INTRASPECIFIC SYMPATRY IN A "RING SPECIES," THE PLETHODONTID

SALAMANDER ENSATINAESCHSCHOLTZII, IN SOUTHERN CALIFORNIA

DAVID B. WAKE, KAY P. YANEV

ofCalifornia,
Zoology,University
Museumof Vertebrate CA 94720
Berkeley,
AND

CHARLES W. BROWN
ofBiology,Santa Rosa JuniorCollege,Santa Rosa, CA 95401
Department

Received December 2, 1985. Accepted March 31, 1986

"Ringspecies,"in whichgeographic distributionis northby twodifferent routes,thelow coastalmoun-

intheformofa circleorring, withoverlapping portions tainsandthehigher inlandmountains. In theabsence
behavingas distinct species,are amongthestrongest ofanyevidenceofhybridization or intergradationin
evidence forgradual divergentspeciationinvolvinglarge the south,he statedthat". . . the terminalraces of the
populationalunits(Cain, 1954; Mayr,1963). There chain,whichcometogether geographically, alreadyap-
are,however, fewexamplesofringspecies, peartobe incompatible
relatively andtohaveattained thespecies
andgiventhecurrent emphasison founder-effect spe- levelin theirrelationsto eachother.Thattheyarenot
ciation(e.g.,Mayr,1982;CarsonandTempleton, 1984), actuallyso regarded is due to theircircuitous connec-
reinvestigation ofringspeciesis needed.We arestudy- tionthrough intergrading forms."
ingoneofthebestknownoftheringspecies,thepleth- An intriguing discoverywas a "trans-valley leak"
odontidsalamander Ensatinaeschscholtzii ofwestern midwaythrough theringofa populationofa coastal
NorthAmerica.For severalyearsa comprehensive unblotched subspecies intotherangeofa blotched sub-
geneticanalysisof patterns of variationand interac- speciesinthecentral SierraNevada.AtJawbone Ridge
tionsofpopulations withinEnsatinahas beenunder- in TuolomneCountybothformswerefoundtogether,
way(Wakeand Yanev, 1986,unpubl.).In thispaper and a presumedhybridindividualwas also found
we report initialresultsfroma southern Californialo- (Stebbins,1957).
calitywhereintraspecific sympatry occurswithno evi- In 1957,Stebbinsreported thediscovery ofa region
denceofhybridization. ofintraspecificsympatry intheSanBemardino Moun-
tainsin southemCalifomia.Bothblotchedand un-
Background blotchedanimalswerecollectedbetween6,100 and
In 1949,Stebbinspublisheda taxonomicrevision 6,300ftinMill(morecorrectly, Sawmill) Canyon, above
ofEnsatina,including a detailedanalysisofgeographic thecityofBanning.Although no intergrade orhybrid
variation incoloration andbodyproportions. Stebbins animalswerediscovered, thecollections werescanty
considered to be a widelydistributed and the need foradditionalworkwas recognized(". . .
E. eschscholtzii
polytypic specieswithseven subspecies,recognized wenowhavean opportunity to discoverifinterbreed-
primarily on thebasisofcoloration. In California,the ingoccursinan areaofseemingly unquestionable sym-
subspeciesare distributed in a ringsurrounding the patry,"Stebbins,1949p. 270).
CentralValley.Unblotched subspeciesintergradewith The situation becamemorecomplexin 1964,when
blotchedsubspeciesaroundthe northern end of the BrownandStebbins reported discovery ofa presumed
valley,and,as one proceedssouthward on eitherside hybrid(andtwospecimens which"seemedto display
ofthevalley,thedifferences incoloration becomemore evidenceofintrogression") in a collectionof 16 sala-
pronounced. In southern California,therangesofthe mandersfromSawmillCanyon.Brown(1974) fol-
inlandblotched andthecoastalunblotched subspecies lowedup thisdiscovery withan extensive analysisof
overlap.Stebbinsthought thatinvasionof southern interactions between theblotched andunblotched sub-
California byancestral populations hadbeenfromthe speciesin theSierraNevada and in southern Califor-

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 NOTES AND COMMENTS 867

nia. He describeda narrowzone of hybridization in has occurred.Ensatina eschscholtziiis stronglydiffer-

theSierraNevadaandestimated thatitcontainedabout entiatedin termsof electrophoretically detectablepro-
8% hybrid animals(basedon hybrid indexanalysisof tein variants (Wake and Yanev, 1986), and we had
In southern
colorpattern). California onlyabout3.5% reason to expect such a study to be fruitful.Tissues
ofanimalsin twohybrid zoneswereconsidered to be (liver,kidney,spleen,heart,and intestine)fromfreshly
hybrids. sacrificed specimens were extracted and frozen at
In hismostrecentstatement on thegroup,Stebbins - 76?C. Carcasses were fixedin formalinand storedin
a single
torecognize
(1985)continues taxonomic species. 70% ethanolin the collectionsof the Museum of Ver-
He comments andunblotched
thatblotched formsco- tebrateZoology.
existin thePeninsularRangesbutthathybridization Combined tissueextractsweresubjectedto horizon-
occursat Mt.Palomarand elsewhere in southernCal- tal starch-gelelectrophoresis(Selanderet al., 1971). We
iformia. surveyed27 proteinsusing standardmethods (details
available upon request; fortypicalgel buffersystems
MATERIALS AND METHODS and proteinssurveyedin thislaboratorysee Yanev and
We haveconductedfieldsurveysin southern Cali- Wake, 1981; Wake and Yanev, 1986). We foundfixed
forniainordertodocument distributionsoftheblotched differences,witha fewminorexceptionsnoted below,
andunblotched Ensatinaand to obtainspecimens for for10 proteins,as follows:superoxidedismutase(SOD),
ourlaboratory studies.In thecourseofthisworkwe phosphogluconatedehydrogenase(PGD), two aconi-
havestudiedfoursitesat whichsympatry ofblotched tase loci (ACON-I, ACON-2), malate dehydrogenase
andunblotched Ensatinaoccurs:SawmillCreekinthe (MDH), peptidase 1-phenylalanyl- 1-proline (PAP),
SanBernardino Mountains, thePalomarMountainre- peptidase 1-leucylglycylglycine(LGG), adenosine de-
gionofSanDiegoCounty(bothareasstudiedbyBrown aminase (ADA-2), alcohol dehydrogenase(ADH-J),
[1974]),the northwestern slopesof the San Jacinto and glucose phosphateisomerase (GPI).
Mountains in RiversideCounty, and CampWolahi,a
RESULTS AND DISCUSSION
privatelyheldenclaveinRanchoCuyamacaStatePark,
SanDiegoCounty. Atthefirst threesites,blotched and No hybridindividuals were found,and thereis no
unblotched forms occurinmicrosympatry, andhybrid evidence of recentintrogression.Individuals hetero-
individualsoccurinlowfrequency. Ourlargest sample, zygoticfor some proteinsare found among both the
144 specimens froma groupofneighboring localities blotched and unblotched samples, but the greatest
in thePalomarMountainregion,includesabout 8% number of heterozygousloci per individual is three
hybrid animals.Onlytwoorthreeofthesecouldbe F1 (two blotchedindividuals).In both individuals,two of
hybrids, basedon allozymeprofiles. Colorpatterns of the threeheterozygoticproteinsinvolve variants ab-
nearlyall hybridsare intermediate betweentypical sentin the unblotchedsample. The heterozygoticpro-
blotchedand unblotched morphs(see Brown[1974] teins of the unblotchedsample (never more than one
forillustrations and descriptions). Detailed electro- per individual) involve only variants absent in the
phoretic studiesarein progress andwillbe reported at blotched specimens, with one exception: one un-
a latertime.Atthefourth site,CampWolahi,no evi- blotchedand one blotchedindividual share a variant
denceofhybridization hasbeenfound.Becausethisis allele forACON-I (as a heterozygotein both) that is
ofspecialinterest to theissueofreproductive closure not foundelsewherein eithergroup.The heterozygotic
andattainment ofspeciesstatus,we present somerel- proteinsoftheblotchedspecimensinvolved onlyvari-
evantdata. ants absent in the unblotchedspecimenswith the fol-
Camp Wolahi,operatedby the Campfire Girls,is lowingexceptions.Four ofthe 42 specimensdisplayed
locatedon thesouthsideofBoulderCreek,alongthe a variantin a heterozygoticstateforLGG thatis fixed
north-facing slopesofMiddlePeak (5,893ftelev.),1 in the unblotchedsample. Two of the 42 specimens
kmto thesouth.The collecting siteis locatedat ap- displayeda variantforPAP thatpredominatesin the
proximately 4,600ftelev.,in a richlydiverse,dense, unblotchedsample; this variantis presentin a homo-
mixedconiferous-hardwood forest.Wehypothesize that zygous state in one specimen and in a heterozygous
theunblotched populations movedintotheareafrom statein anotherof the blotchedsample. We examined
lowerelevationsbyfollowing riparianwoodlandthat a number of populations of blotched Ensatina from
linesBoulderCreek.Thislocalityis thesouthernmostnearbyareas but have not found eitherof the excep-
siteofsympatry in thegenus. tionalvariantsmentionedabove. However,our sample
Blotchedandunblotched salamanders werefoundat sizes are not large,and we cannot dismiss the possi-
CampWolahiin thewinter of 1982.Subsequently we bilitythattheseare simplylow-frequencyvariants.To
established a lineofpitfalltrapswhichhas beenef- state this in a different way, thereare 50 (the sample
fective.Typical unblotchedEnsatina eschscholtziisize) x 2 (these are diploids) x 10 (the numbers of
eschscholtzii and typicalblotchedE. e. klauberihave proteinsreported),or 1,000 variants (which we pre-
beentakenin microsympatry, withina fewcmofeach sume forthe purposesof thisanalysisto be equivalent
other,and we havehad no suggestion fromcolorpat- to codominantalleles) in our sample fromCamp Wo-
ternthatany hybridization has takenplace. At this lahi. One of these 1,000 variants is of questionable
site,wehavedetected no obviousdifferences inhabitat originin the unblotchedsample and eight are ques-
preferences. In general,eschscholtzii elsewhere favors tionable in the blotched sample. Thus, at most,fewer
lower,moreopen habitatsthanklauberi,and more than 10, or about 1%, of the variantsin our sympatric
openhabitatsthanoccurat CampWolahi. sample could be the resultof introgression.Given the
We examinedproteinvariationin eightunblotched lack of concordanceamong the heterozygoticproteins
and 42 blotchedsalamanders, to determine whether involving questionable variants, any introgression
introgression (whichwe areunableto detectvisually) would have to have been the result of very limited

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868 NOTES AND COMMENTS

hybridization at some relatively distanttimein the LITERATURE CITED

past. BROWN, C. W. 1974. Hybridizationamong the sub-
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andunblotched populations atCampWolahirepresent eschscholtzi.Univ. Calif. Publ. Zool. 98:1-56.
distinct
biologicalspecieswhicharenotnow,andhave BROWN, C. W., AND R. C. STEBBINS. 1964. Evidence
notin therecentpast,engagedin anyhybridization. for hybridizationbetween the blotched and un-
Subsequent totheelectrophoretic survey reportedhere, blotched subspecies of the salamander Ensatina
oursamplehasgrown to 10unblotched and76 blotched eschscholtzi.Evolution 18:706-707.
specimens, noneofwhichshowanyexternal evidence CAIN, A. J. 1954. Animal Species and Their Evolu-
ofhybridization. tion. HutchinsonUniv. Library,London, U.K.
Theconceptofa ringspeciesis appropriately applied CARSON, H. L., AND A. R. TEMPLETON. 1984. Genetic
to Ensatina.A chainofmorphologically distinctsub- revolutionsin relationto speciationphenomenon:
species,each intergrading withits neighbor, has ter- The foundingof new populations. Ann. Rev. Ecol.
minalpartswhichoverlapand betweenwhichgene Syst. 15:97-131.
flowis slightto nonexistent. At Camp Wolahino in- MAYR, E. 1963. Animal Species and Evolution. Har-
termediate colorpatterns areseen,andno geneticevi- vard Univ. Press, Cambridge,MA.
denceofhybridization is found.The twomorphsare 1982. Processes of speciationin animals,pp.
reproductively isolatedfromeach otherand havethe 1-19. In C. Barigozzi (ed.), Mechanisms of Specia-
statusofbiologicalspecies. tion. Liss, NY.
The existence ofthechainofintermediate popula- SELANDER, R. K., M. H. SMITH, S. Y. YOUNG, W. E.
tionsextending in a giantringbetweentheterminally JOHNSON, AND J. B. GENTRY. 1971. Biochemical
overlapping populations ofEnsatinaleads to a taxo- polymorphismand systematicsin the genus Pero-
nomicproblem.For thepresent, we continueto rec- myscus.I. Variation in the old fieldmouse (Pero-
ognizea singletaxonomic species.Workin progress is myscuspolionotus).Univ. Texas Publ. Stud. Genet.
directedexplicitlyat theintergradation zonesandwill 6:49-90.
investigatethepossibility thatgeneticinterchange is STEBBINS, R. C. 1949. Speciation in salamanders of
notas continuous as geographic variationin colorpat- theplethodontidgenusEnsatina. Univ. Calif.Publ.
ternsuggests. Zool. 48:377-526.
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salamander Ensatina eschscholtzi.Evolution 11:
ACKNOWLEDGMENTS 265-270.
We thank the CampfireGirls and the manager of 1985. A Field Guide to WesternReptilesand
Camp Wolahi, Tom Ruzich, forpermissionto study Amphibians. Houghton Mifflin,Boston, MA.
salamanderson theirproperty.Monica Frelowassisted WAKE, D. B., AND K. P. YANEV. 1986. Geographic
in all phases of the laboratorywork and conducted variationin allozymesin a "ringspecies," thepleth-
most of the electrophoresis.We have been assisted in odontidsalamanderEnsatina eschscholtziiof west-
fieldworkby manyindividuals,but especiallythe fol- em North America. Evolution 40:702-715.
lowing:R. Marlow, M. Wake, S. Sweet,J. Hanken, J. YANEV, K. P., AND D. B. WAKE. 1981. Genetic vari-
Cadle, S. Haskins,D. Good, T. Papenfuss,and R. Ma- ation in a relict desert salamander, Batrachoseps
cey. Allen Larson, Nancy Staub, and Kiisa Nishikawa campi. Herpetologica37:16-28.
provided helpfulcommentson the manuscript.This
researchwas sponsoredby NSF (GrantBSR 8305763). Corresponding Editor:J.A. Endler

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