Repeated Evolution of Sexual Color Dimorphism in Passerine Birds

The Auk 113(4):842-848, 1996

REPEATED EVOLUTION OF SEXUAL COLOR DIMORPHISM IN PASSERINE BIRDS

TREVOR PRICE • AND GEOFFREY L. BIRCH Departmentof Biology0116, University of Californiaat SanDiego, La Jolla,California 92093, USA

ABSTR•CT.--Wepresent a surveyof passefinebirds designed to investigatethe frequency with which sexualdimorphism in colorationor color pattern has evolved from monomor- phisin(or the converse).Based on the numberof generathat haveboth a monomorphicand a dimorphicspecies, and the minimumnumber of changesinferred to haveoccurred between genera,the transition between dimorphismand monomorphismhas occurredat least 150 times.Using the Sibley/Ahlquistphylogeny, we obtain maximumlikelihood estimatesof the probabilitythat one statewill be in the other after one million yearsof 0.01 to 0.02 (monomorphismto dimorphism)and 0.03to 0.04(dimorphism to monomorphism).The rate of transitionfrom dimorphismto monomorphismappears to be higher than the converse, and there are more monomorphicthan dimorphic species.We concludethat the transition betweenalternative states is notdifficult, and that the evolutionof sexualdimorphism, given appropriateselection pressures, is unlikelyto beconstrained. Received 15 August 1995, accepted I April 1996.

MANYSPECIES OF BIRDS are sexuallydimorphic iceus),suggests that correlatedresponses do oc- in color or color pattern. This often is thought cur (Muma and Weatherhead 1989). However, to be a consequenceof sexual selection, and rudimentaryfemale traits,at leastin somespe- sexualdimorphism in color has been usedas an cies, may be maintained at their observedlevel index of the intensity of sexualselection in com- of expressionby selection.Several analyses have parative studies (Hamilton and Zuk 1982, Read implicated selectionon female plumagesas a and Harvey 1989,Fitzpatrick 1994,Moller and main cause of the presence or absenceof di- Birkhead 1994, Barracloughet al. 1995). Popu- morphism (Bj6rklund 1991, Irwin 1994). lation studieshave confirmed that male plum- Therefore, the degreeto which the evolution age patterns in sexually dimorphic speciesare of dimorphismis limited or preventedby a high subject to sexual selection (Price 1984, Moller genetic correlation between the sexesremains 1989, Hill 1990, Petrie and Halliday 1994),and unclear.In this paperwe estimatethe minimum Moller and Birkhead (1994) show that dimor- number of times dimorphism has evolved in phisin is correlatedwith the frequencyof ex- the Passeriformes. We find it has evolved at trapair copulationsacross species. least 150 times.We suggestthat this is a high The evolutionof sexualdimorphism requires number,and that the evolution of dimorphism not only appropriateselection pressures but also from monomorphism (or its converse,mono- sufficientgenetic variation. Lande (1980) sug- morphismfrom dimorphism)is not constrained gestedthat the evolution of sexualdimorphism greatly by an absenceof genetic variation for might be constrained,because many of the genes dimorphism. affectingvariation in malessimilarly affect variation in females. Selection on males therefore METHODS resultsin a high correlatedresponse in females, and sex-limitation may require many genera- Throughout this paper, monomorphismand di- tions of selectionto separatethe expressionof morphism are used as shorthand for sexual monoch- romatism and sexual dichromatism. The trait "sexual thosefew genesthat affectthe male and female dimorphism"is particularlysuitable for study be- differently. The presenceof rudimentary male causeof the many specieswhose phenotypic state is traits in females, such as reduced epaulets in known. Therefore,even low frequenciesof transition female Red-wingedBlackbirds (Agelaius phoen- between states should be detectable. We do not con- sidersexual dimorphism in size,or in ornamentssuch as wattles,plumes, and elongatetails. E-mail: [email protected] We studiedthe 5,398 passerinebird speciesin the

842 October 1996] SexualDimorphism in Birds 843 100 171 157 135 98 51 20 1,125 genera listed in Clements' (1981) check-list of E 439 birds of the world. A more recent list by Sibley and • 80 Monroe (1990) is similar to Clements in the classification of speciesto genera (but with 5,705 speciesin 1,164genera), and the resultsare identical regardless c• 6o of which compilation is used. Using field guides,we were able to determine the presenceor absenceof sexualdimorphism in color or color pattern for spe- • 4o cies in all but 54 of the genera (66 species).We classified a speciesas sexually dimorphic if the sexeswere •O 20 describedseparately in species'descriptions, or if the sexesappeared different in illustrations. Therefore, •' 0 minor differences,such as more spotson a larger bird, I 2 3-4 5-8 9-16 16-32 >32 would not be counted. Nevertheless,the degree of dimorphismvaries from strongto mild. Examplesof NUMBER OF SPECIES IN GENUS specieswith weak sexualdimorphism are the Tropical FIG. 1. The proportion of passerinebird genera Parula (Parulapitayumi), in which the female lacksthe containing all mononaorphic(filled squares),all di- male'sorange breast band, and the White-browedTit- morphic(open squares ), or mixed mononaorphicand Warbler (Leptopoecilesophiae), in which the female is dimorphicspecies (filled circles)for generawith dif- paler and without much of the male's blue wash. ferent numbersof species.Numbers of generain each Speciesthat are seasonallydimorphic (e.g. Scarlet classare listed at the top of the figure. Tanager [Pirangaolivacea]) were classified as dimorphic, whereasthose with polymorphismsthat are not sex limited (e.g. Scaly-breastedWren-Babbler [Pneo- mateof relationshipsamong genera currently avail- pyga albiventer],All and Ripley [1983]; and several able. Using parsimonywe then reconstructedances- Wheatear species[Oenanthe], Mayr and Stresemann tral stateson the tree using the ACCTRAN method [1949]) were classifiedas mononaorphic.We did not (Maddison1989). This gives a single parsimonious record the plumage state of every species,but rather estimate,and there may be other equally parsimo- whether a genusconsisted entirely of mononaorphic nious trees (Maddison 1989). We did not search for species,entirely of dimorphic species,or a mixture. these becausewe were interestedmainly in estimat- Therefore, we are unable to place an exact figure on ing minimum frequencyof change.The method as- the proportion of all speciesthat are mononaorphic. signs each node below the tips of the tree as mono- We estimatethat at least 60% of all speciesare monomorphic (M), dimorphic (D), or mononaorphicor dimorphic (Fig. 1). Barracloughet al. (1995),in a smaller morphic(M/D) dependingon the stateof the genera sample of passerines,found that 69% were mono- above the node. One then works down the tree scor- morphic.Some species may be crypticallydimorphic ing eachnode according to the statesof the two nodes in ultraviolet light, in which casethe number of di- above(e.g. if the two nodesabove were M/D and D, morphic specieswould be underestimated.However, the node below is D). Finally, when all nodes had no specieshas been discoveredto be sexuallydimor- been assignedwe worked back up the tree assigning phic in ultraviolet light but mononaorphicto humans, M/D nodes as M or D depending on their inferred despite an extensive search (Staffan Andersson pers. ancestor. After all nodes had been reconstructed as comm.). mononaorphicor dimorphic, we tallied the number The main goal of the study was to estimate the of transitions between the two states. frequencyof transitionsbetween monomorphism and If changehas been frequent,parsimony is likely to dimorphism.To do this we used two approaches,i.e. produce a gross underestimateof the number of within generaand among genera. changes.For example,in the extremecase of a change Within genera.--We tallied the number of genera in state at every speciationevent, parsimony will re- containingboth a mononaorphicand a dimorphicspe- suit in a constructionwith no change below sister cies, excluding from considerationspecies that are pairs at the tips of the tree. Therefore, we used the both mononaorphicand dimorphic in different parts maximum likelihood method of Pagel (1994) to di- of their range. If genera are assumedto be mono- rectly estimatefrequency of change.The method ob- phyletic, then each genuscontaining both a mono- tains those probabilitiesof change from mononaor- morphic and a dimorphic speciesrepresents an in- phic to dimorphic and from dimorphic to mononaor- dependent evolutionary transition between the two phic that maximize the probability of the observed states. statesat the tips of the tree. The main assumptionis Amonggenera.--We located 399 of the genera on that the probability of changeper unit branch length Sibley and Ahlquist's(1990) phylogenetic tree based is constantthroughout the tree. We assumedthat the on DNA-DNA hybridization data. The tree clearly Sibley-Ahlquisttree and associatedbranch lengths will have inaccuracies,but it providesthe best esti- were a given parameter. Branch-lengthswere mea- 844 PRICEAND BIRCH [Auk,Vol. 113 suredwith a ruler. We usedall 594 tips in the phy~ timate of the probability that a dimorphic spe- logeny as input, so that when severalspecies for one cieswould be monomorphicafter 1 million years genuswere separatelyplaced on the tree they were varied from 3.4 to 4.4%. These estimates are con- treated separately.There were 26 tips for which we founded by many uncertainties,but they are were unable to identify plumagestate of the species consistentwith the within-genera patternsin or genus.For thesetips we boundedthe estimatesby running the program assuming these tips were all indicating a moderately high rate of change. monomorphicand in other runs by assumingthem Asymmetricalevolutionary rates.--Our analyses to be all dimorphic. There also were 22 tips where imply that changebetween statesof monomor- Sibleyand Ahlquist list a genusname, and the genus phisin and dimorphism is sufficiently "easy" containsboth monomorphicand dimorphic species. and not ultimately constrained.It is of interest We ran the programin three ways,assigning the tips to askwhether dimorphismevolves into mono- to be monomorphic, dimorphic, or to consistof two morphism at a different rate than vice versa. species,one of which is dimorphic and the other Using the parsimony method, 227 ancestral monomorphic.In the latter case,the two specieswere nodeswere reconstructedas monomorphic, with separatedby a branch with the same length as that separating their genus from their sister genus. The 11 (4.8%) subsequentmonomorphic-to-dimor- branchlength separatingthe node joining thesetwo phic transitions, and 136 nodes were recon- speciesfrom the sistergenus was assigneda length structedas dimorphic, with 9 (6.6%)subsequent of zero. Becausethe Paget program requiresa fully dimorphic-to-monomorphictransitions. This resolvedtree, all branch lengths of zero (including gives an estimated per-lineage transition rate thoseresulting from potytomieson the tree) were re- from dimorphism to monomorphism 1.4x assigneda small value (i.e. 0.1, where branchlength higher than the converse (the term lineage variesup to 58 ram). The programestimates transition meansthe line connectingan ancestralspecies rates between the two states. We used formulae in with one of its descendants). The difference is Paget (1994) to convert these rates into estimatesof not significant (X2 = 0.2, df = 1, P > 0.05). the probability that a speciesin one state would be The taxonomictreatment may be interpreted in the other state ! million yearslater. Branchlength was convertedinto time following the passerinecal- as indicating a higher rate of transition from ibration usedby Sibteyand Ahlquist (1990). dimorphism to monomorphism than the converse.The plot of the proportionof generacon- taining both monomorphicand dimorphic spe- RESULTS ciesagainst number of speciesin the genusrises from zero (as it must when there is only one Patternswithin genera.--Monomorphism to di- speciesin the genus) to 45% for those genera morphism (and vice versa) transitionshave oc- containing many species(Fig. 1). The increase curredfrequently; 130 passerine genera contain in mixed genera appearsto be more at the ex- both monomorphicand dimorphic species,im- penseof dimorphicthan of monomorphicgen- plying at least 130 transitions (Fig. 1). Among era (Fig. 1). The unweighted regressionslope the 304 passerinegenera with five or more spe- of the seven points in Figure 1 for monomor- cies, 46% are entirely monomorphic,22% are phic genera is fl = -0.03 + SE of 0.006. For entirely dimorphic,and 32%contain at leastone dimorphic genera the slope is steeper,i.e. fl = monomorphicand one dimorphicspecies. These -0.05 + 0.007. The steeper slope for the di- 32% directly reflect at least one transition, and morphic genera appearsto be mainly because they imply that transitionsbetween monomor- the very speciosegenera (thosewith > 15 spe- phisin and dimorphismare frequent. cies) rarely consistentirely of dimorphic spe- Patternsbetween genera.--Using parsimony, we cies.We used a test to comparethe numbersof found a minimum of 11 cases of an inferred one-speciesgenera that are monomorphic or monomorphic-to-dimorphic transition along dimorphic (269 vs. 170) with the numbers of internal branches of the Sibley/Ahlquist tree, genera containing > 15 speciesthat are either and 9 casesof an inferred dimorphic-to-mono- all monomorphic or all dimorphic (32 vs. 9). morphic transition. Relatively more of the speciosegenera are Maximum likelihood estimates.--The estimate monomorphic(X 2 = 3.8, df = 1, P < 0.05). One of the probability that a monomorphicspecies explanationfor this resultis that dimorphicspe- would be dimorphicafter 1 million yearsvaried cies are quite likely to give rise to a monomor- from 1.1 to 1.6%,depending on how unknown phic descendant(and thus the genus of which tip specieswere coded (seeMethods). The es- the speciesis a member becomesclassified as October1996] SexualDimorphism in Birds 845

"mixed" rather than purely dimorphic).If this curred. When traits evolve frequently there is occurs,then speciosegenera should more often a tendency for parsimonyto grosslyunderes- be mixed or pure monomorphic than they timate the frequenciesof change lower down should be dimorphic, at least when these spe- the tree,and parsimoniousestimates place much closegenera are contrastedwith thosecontain- of the changein the tips of the tree, as is seen ing few species. here. Accordingly,we used an alternativeas- The maximum likelihood method estimates sumption that the probability of change give a rate of change from dimorphism to throughout the tree has been constant,but we monomorphismapproximately 3 x higher than placedno restrictionon how large that change the rate from monomorphism to dimorphism, has been. Under this assumption, estimated but we cannoteasily assessthe statisticalsig- probabilitiesof transitionsbetween states range nificanceof this result, given a variety of dif- from 0.01 to 0.04 per speciesper million years. ferent sourcesof error. The parsimony,likeli- Among passerines,females are never obvi- hood, and taxonomic treatments all are consis- ouslybrighter-plumaged than males.The tran- tent with there being a higher per-lineagerate sition between dimorphism and monomor- of transition from dimorphism to monomorphism can result from male evolution (i.e. a phism than the converse,but at least two alter- bright plumageis gainedduring the evolution native explanationsexist. First, the taxonomy of dimorphism from monomorphism, or lost method relies on classificationsof dimorphic during the evolution of monomorphism from speciesto genera being basedon the samecri- dimorphism). Alternatively, the transition can teria as the classificationof monomorphicspe- be due to female evolution (i.e. a bright plum- ciesto genera.Second, and more generally, our age is gained during the evolution of mono- interpretation depends on the assumptionthat morphismfrom dimorphism,and lost during the expectedper-lineage transition rate is a con- the evolution of dimorphism from monomor- stant.It is easyto comeup with scenarioswhere phism; BjSrklund 1991, Irwin 1994). transition rateshave varied in different parts of We have not attemptedto classifymonomor- the tree so that the rate of changefrom dimorphic speciesas dull or bright becauseof the phism to monomorphismis not higher in one obvioussubjectivity in suchclassifications. For part of the tree than in any other part. For ex- example,very bright birds may appear cryptic ample, some groups could have stayed mono- in their natural backgrounds.However, com- morphic with no transitions between either parisonsof dimorphic and monomorphic pop- state,while otherscould have rapidly changed ulationswithin a singlespecies can be usedto betweenthe two states,with equal probability. unequivocallyidentify monomorphicpopula- When averagedacross all lineages,the rate of tions as relatively dull (like the female of the change from dimorphism to monomorphism dimorphic population)or bright (like the male will be higher than the converse.Because sce- of the dimorphic population). In an important narios such as these are based on a posteriori paper, Peterson (1996) surveyed geographic inspection of those groups currently mono- variation in sexual dimorphism within species morphic,they cannotbe rejectedwith statistical and superspeciesgroups. Within the passerines, methods. Peterson lists 36 species or superspeciesthat have both monomorphic-dull and dimorphic DISCUSSION populations,27 speciesor superspeciesthat have both monomorphic-brightand dimorphicpop- Our most striking result is that sexual di- ulations, and two speciesor superspeciesthat morphism and monomorphism have evolved havemonomorphic-bright, monomorphic-dull, repeatedlyone from the other. We have iden- and dimorphic populations(Peterson also lists tified 130 cases of transitions between mono- many additional examplesof geographicvari- morphism and dimorphism basedon the num- ation in the degree of dimorphism). Casesof ber of genera containing both a monomorphic sexualdimorphism evolving within speciescan and a dimorphic species,and 20 deeper in the be used to determine directions of evolution phylogeny,giving a total of 150cases altogeth- (by comparingthe monomorphicwith the di- er. This is expected to be a minimum estimate morphic population). Among those species of the actual number of times that the dimor- showinggeographic variation in dimorphism, phism/monomorphism transitions have oc- monomorphic-dull populations are about as 846 PeaceAND BIRCH [Auk,Vol. 113 frequent as monomorphic-bright populations, ly part of their life males resemble females and implying that female change drives the evo- only later acquirea characteristicadult plumage lution of sexual dimorphism about as often as (Rohweret al. 1980).In thesespecies, relatively does male change (Peterson1996). early breeding easily could result in the lossof The main conclusion that transitions between the distinctive adult male plumage, and hence alternative stateshave occurred quite common- monomorphism (Lawton and Lawton 1988).This ly is unlikely to have been greatly affectedby explanation applies to the loss of distinctive errors of classification.Although genera may male plumages, but not to the gain of bright not always represent monophyletic groups, plumagesby the female. many species'pairs that differ in state clearly There appearsto be little absoluteprohibition are close relatives of one another (e.g. the on the evolution of sexual dimorphism.Nev- monomorphic Tree Sparrow [Passermontanus] erthelessa high geneticcorrelation between the vs. the dimorphic House Sparrow [Passerdo- sexes could restrict the evolution of dimor- mesticus]). Similarly, at among genera, the phism. First, direct selection on males for in- monomorphic, dimorphic, and mixed genera are creased coloration can cause the females to be- interspersedacross the tips of the Sibley-Ahlqu- comebrighter as a correlatedresponse. Bright- ist phylogeny. Errors in the topology are most ness in females, and hence monomorphism, likely to affect nearby groups, and they make subsequentlycould be maintained by newly little difference to the inference that transitions arising selectionpressures on females,such as between monomorphismand dimorphism have male choice (Hill 1993, Jones and Hunter 1993, been quite common. Peterson's (1996) docu- Wynn and Price 1993), nonbreeding social in- mentation of the large numbers of speciesthat teractions (West-Eberhard 1983, Irwin 1994), or show geographical variation in degree of di- sexual selection involving female competition morphism strengthens the conclusion that di- and/or mimicry of the oppositesex (Trail 1990). morphism can evolve readily. Second, if sexual selection pressuresare non- The ease with which monomorphism (or di- specific,and traits such as male song or court- morphism) can evolve suggests that genetic ship are equally suitablealternatives, then traits constraints are not strong. Dimorphism can with the high sex-limitedgenetic variance may evolve only if genetic variation is sex-limited, be the most likely to invade and become estab- and sex-limitation may arise from two causes. lished in the population. Once one male trait First, mutations may occur on the sex chro- has becomeestablished, other traits may be less mosome. Dosage compensation appears not to likely to spread (Lande 1981, H6glund 1989, occur in birds (Baverstocket al., 1982), so these Schluter and Price 1993). mutations will automaticallybe expresseddif- When averaged acrossthe whole tree, the ferently in males and females. Such sex-linked per-lineage rate of transition from dimorphism mutations are known from chickens (Hutt 1949). to monomorphism apparently is higher than Second,some autosomalgenes may be subject the converse, and monomorphic species are to sex-limited expression (Fisher 1958, Lande more frequent than dimorphic species.Barra- 1980). For example the expressionof somecol- clough et al. (1995) usethe Sibley/Ahlquist tree ors in the male is dependent either on the pres- to showthat speciationrates are higher in clades ence of testosteroneor the absenceof estrogen with a higher frequency of dimorphic species, (Witschi 1961, Owens and Short 1995). Selec- and they suggestthat this is a result of sexual tion to change coloration in one sex will then selectionpromoting both dimorphism and spe- eventually lead to the evolution of dimorphism, ciation. Therefore, differential speciationrates although the processmay be very slow (Lande might lead to an increasein dimorphic species, 1980). which could be opposedby the higher rate of One way that dimorphism may evolve rap- evolution from dimorphismto monomorphism. idly is if selectionacts to changeother sex-lim- Alternatively, somegroups may tend to remain ited traits (such as levels of testosterone) that monomorphic with low speciationrates, where- have pleiotropic effectson color or pattern. Col- as other groups are sexually selectedand have or will evolve as a correlated response,and all both high speciationrates and a high frequency changeswill be restricted to one sex. For ex- of transitionsbetween monomorphismand di- ample, some dimorphic bird speciesexhibit de- morphism. 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REVIEWERS FOR THE AUK, 1996

The review processis essentialto the main- Cooch,Brian A. Cooper,John C. Coul$on,Al- tenanceof high scientificstandards in a journal. exander Cruz, Robert L. Curry*, Thomas W. The efforts of individual referees are remark- Custer, Francesca J. Cuthbert, C. Brad Dabbert, able, and we take this opportunityto acknowl- Richard DeGraaf, Patricia Deibert, Kim C. Der- edge publicly those who contributed reviews rickson, Randy Dettmers, Pierre J. Deviche, during the periodthat Volume 113was in prep- Andre A. Dhondt, Terri Donovan, Ronald D. aration. The memorials were solicited and man- Drobney, Sam Droege, Tom Drummer, Paul J. aged by C. Stuart Houston. Individuals who DuBowy,David C. Duffy, Alfred M. Duffy, Pe- contributed two or more reviews are signified ter O. Dunn*, JohnB. Dunning*, JohnM. Eadie, with an asterisk. Laurie S. Eberhardt, Marcel F. Eens, Steve Em- David G. Ainley, Rauno V. Alatalo, Jeff Al- slie, David A. Enstrom,David L. Evans,Roger berts,Ray Alisauskas,Marc W. Allard, JavierA. M. Evans*, John R. Faaborg*, Daniel P. Faith, Alonso, Daniel Anderson, C. Davison Ankney, GregH. Farley,J. Alan Feduccia,Millicent Fick- RobertG. Anthony, PeterArcese, Todd Arnold, en, Frank Fish,John W. Fitzpatrick*, JonFjeld- Goran Arnqvist, RobertA. Askins*, JonathanL. s•i, Lester D. Flake, Paul L. Flint, Alan B. Frank- Atwood, Alexander Badyaev*, Franz Bairlein, lin, Lindy N. Garner,Kimball L. Garrett,Sidney Allan J. Baker, Guy A. Baldassarre,Winston E. A. Gauthreaux*, Frederick R. Gehlbach, T. Luke Banko, Richard C. Banks, George F. Barrow- George,Cameron K. Ghalambor,H. LisleGibbs, clough*,John M. Bates*,Kathleen G. Beal,James Frank B. Gill, Travis C. Glenn, Bruce Glick, Mi- C. Bednarz*, Peter A. Bednekoff, Marc Bekoff*, chael Gochfield, David L. Goldstein, Patricia A. LeslieD. Beletsky,James R. Belthoff,Craig W. Gowaty*, Gary R. Graves, Russell S. Green- Benkman, Herman Berkhoudt, Louis B. Best*, berg*, JeremyGreenwood, Jeff Groth, Thomas C. J. Bibby, John W. Bickham,John G. Blake, C. Grubb, Jr., JosephA. Grzybowski*, Susan RobertE. Bleiweiss,David A. Boag,Peter T. Boag, Haig, Jack P. Hailman, Paul B. Hamel, H.T. WalterBock, Johan J. Bolhuis, Mark Bolton,Gary Hammel, Yves Handrich, J. W. Hardy, M.P. R. Bortolotti*, Clait E. Braun, Jeff Brawn, Rand- Harris*, Richard G. Harrison, Ian Hartley, S. D. all Breitwisch,Mark Brigham,I. L. Brisbin,James Healy, Carl Heine, Paul Hendricks, JamesR. V. Briskie, M. de L. Brooke, Charles R. Brown*, Herkert, Geoffrey E. Hill*, Keith A. Hobson, Jerram L. Brown, Joel S. Brown, Robert B. Brua*, JacobHoglund, Richard T. Holmes, Robert W. Dianne H. Brunton, Enrique H. Bucher, Joanna Howe, JocelynHudon, Peter J. Hudson, Philip Burger,Gregory S. Butcher,Robert W. Butler*, S. Humphrey, JerryW. Hupp, Victor H. Hutch- Ronald G. Butler, Tom J. Cade, William A. Cal- ison, Richard L. Hutto, Danny J. Ingold, Re- der, Des Callaghan,Cynthia Carey*, JayH. Car- becca E. Irwin, Jerome A. Jackson, Frances C. ter III, Carel ten Cate, Philip C. Chu, Roger B. James*,Sue Jarvi, Robert L. Jarvis, JosephR. Clapp, Keith Clay, Dale H. Clayton, Martin L. Cody,Charles T. Collins,Kelvin F. Conrad,Evan (continuedon p. 857)