Evolution of Social Organization and Life-History Patterns Among Grouse Author(S): R

Home , Hazel grouse, Lyrurus

Evolution of Social Organization and Life-History Patterns Among Grouse Author(s): R. Haven Wiley Source: The Quarterly Review of Biology, Vol. 49, No. 3 (Sep., 1974), pp. 201-227 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/2822821 . Accessed: 29/07/2011 11:26

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http://www.jstor.org EVOLUTION OF SOCIAL ORGANIZATION AND LIFE-HISTORY PATTERNS AMONG GROUSE

BY R. HAVEN WILEY

Departmentof Zoology, University of NorthCarolina, Chapel Hill, N.C. 27514

ABSTRACT

Correlationsof social structure,life-history patterns, and ecologyamong theseventeen species of grouse exemplifysome general patternsin the evolutionof matingsystems among higher vertebrates.The speciesof grousediffer in theaggregation of displayingmales, the permanence of heterosexualaffiliations, the contributionsof males to parentalcare, and the breedingsex ratio. Promiscuousspecies (no durableheterosexual affiliation) are probablyall polygynous(the breedingsex ratio less thanunity), but fall into twogroups depending on whetherthe displaying males congregateat leks or disperserelatively evenly. In all of thesepromiscuous, polygynous speciesand in threemonogamous species, the female cares for the young;dual parentalcare appearsonly in one monogamousspecies. During theirfirst year, the males of polygynous species do notmate or matemuch less frequently, althoughfemales normally breed at one year of age, a situationtermed sexual bimaturism.At leastamong birds and mammals,polygyny is normallyassociated with sexual bimaturism.Sexual bimaturismand polygynyamong grousecorrelate well bothwith large overallsize, as indicated byfemale weight, and withgreater sexual dimorphismin weight.These correlationsalso recur in othervertebrate families. Among the promiscuous grouse, the dispersion patterns of displaying males probablyrelate to the differencesin predationpressures in open and forestedhabitats. In contrastwith some otheravian families,differences in social structureamong grousehave littlerelationship to majordifferences in diet. Single parentalcare is not a sufficientcondition for the evolutionof polygynyamong grouse. The associationof sexual bimaturismwith polygyny requires, in addition,an explanationof theadaptive advantages of deferredreproduction among males.Postponed reproduction by males will reducethe spread of theirgenes in a populationunless compensated by a sufficientgain in earlysurvival or increasedfecundity later. Calculations of ratesof reproductiveincrease for hypotheticallineages of males indicatethat these compensating conditions can plausiblyexplain theevolution of delayedreproduction among male grouse. Theoreticalconsiderations further suggest that larger size couldfavor the evolution of deferred reproduction,especially in males,and thuscould contribute to theevolution of sexual bimaturism and polygynyin the larger speciesof grouse.Ecological circumstances,including the details offood dispersion, could thusinfluence the evolution of matingsystems indirectly, through effects on theevolution of bodysizes. As polygynyamong higher vertebrates is normallyassociated with sexualbimaturism and is incompatiblewith full dual parentalcare, polygyny should evolve under ecologicalconditions in whichthe adaptive advantagesof sexual bimaturismoutweigh those of dual parentalcare.

INTRODUCTION pioneering evidence for the adaptedness N NLY RECENTLY has it become interspecificdifferences in social organization, Oclear how intricatelya species' social and subsequent studies have explored this organizationis adapted to ecologi- theme further(Crook, 1964, 1965, 1970; Eisen- cal circumstances.Studies by Crook berg, 1966; Lack, 1968; Orians, 1969, 1972; (1962) and Orians (1961) provided Crook and Goss-Custard,1972; Selander, 1972;

201 202 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49

Eisenberg, Muckenhirn, and Rudran, 1972). repeatedly confirmed their close relationships Especially fruitfulhave been investigationsof (Sibley, 1957; Short, 1967). Yet aside fromthe related species that differ markedly in social five traditionally polytypic genera (Lagopus, structure. Tympanuchus,Tetrastes, Tetrao, Lyrurus), the Among birds, the grouse (Tetraonidae) pro- species are not easily grouped. It seems possible vide unusual opportunitiesfor such compari- that some nine or ten phyletic lines radiated sons. The range and gradationsof social struc- fromearly tetraonidancestors, so thatattempts ture among these seventeen species are proba- to identifyonly a few phyletic groups would bly not surpassed in any other avian family. prove illusory.Any similaritiesin social behavior Particularlystriking is the spectrum of mating among the recognized congeneric species pro- systemsamong grouse, ranging frommonoga- vide only equivocal evidence for adaptation. my to extreme polygyny.Yet the hypotheses Also the similaritiesbetween Canachites and developed to explain the adaptedness to social Falcipennis and probably those between systemsin passerine birds, while applicable in Tympanuchusand Pedioecetesare likelyto depend part to grouse, do not provide complete expla- heavilyon common ancestry(Short, 1967). nations for the evolution of their societies. For example, the relationshipof mating systemsto RADIATION OF GROUSE SOCIAL SYSTEMS strategiesof parental care is less clear than in certain passerine families. The social systemsof grouse comprise three The grouse also illustratea general problem general categories, differentiatedon the bases in the evolutionof polygynousmating systems. of the dispersion of displaying males during A widespread correlate of polygyny,at least the breeding season and the duration of het- among birds and mammals, is the later onset erosexual associations (Hjorth, 1970): (1) of reproduction among males than among fe- promiscuity,with males aggregated at leks; (2) males. Grouse exemplifythis correlation well. promiscuity,with dispersed males; (3) mono- The evolutionof polygynyin grouse also seems gamy,with dispersed males (Table 1). As Hjorth inseparable from the evolution of large body (1970) has reviewed much of the literatureof size. The ecological consequences of both of grouse behavior, the present discussion will these featuresmust contributeto the evolution compare more systematicallycertain critical of theirsocial systems.In thisreview a systematic featuresof tetraonidsocial systems,particularly comparison of grouse social systems and an territorialbehavior, interactionsbetween the examination of the correlationsbetween social sexes, and age-related differencesin behavior. structureand otherattributes will allow a closer The term polygamyis used in this paper to analysis of the coevolution of mating systems, denote an unequal sex ratio among breeding body sizes,and sexual differencesin lifehistory. individuals (termed the breedingsex ratio). If more individual females than males contribute one COMMENTS ON METHODOLOGY gametes to zygotesduring any season, the matingsystem is furtherspecified as polygyny. By deducing the ecological consequences of Thus the words polygamy and polygynywill differencesin social behavior and its correlates, here imply nothing about the duration of the one can begin to specifythe selection pressures heterosexual association. The term promiscuous that bear on the evolution of these differences. describes a mating systemin which no prefer- When constellationsof correlatedtraits coincide ential bonds unite individuals of opposite sex. with phyletic groups, however, the possibility Sexual bonds are easily recognized when indi- exists that these similaritiesdepend primarily viduals coordinate their behavior or remain in on the common ancestryof the species, rather close spatial proximityfor an appreciable length than on currentadaptation. If natural selection of time. But less noticeable sexual affiliations in similar environments has resulted in the mightalso occur. An individual mightdevelop evolution of similarlycoordinated adaptations, a preference for mating with a particular these correlations should recur in separate partnereven thoughtheir associations are brief, phyleticgroups. and such preferencesmight not prove recipro- Within the Tetraonidae phyleticgroups are cal. On the otherhand, an apparent preference difficultto distinguish.Systematic studies have could arise when two individuals share attach- SEPTEMBER 1974] EVOLUTION AMONG GROUJSE 203

TABLE 1 SpeciesThat FormLeks (CategoryI) Categoriesof social structureamong grouse The five adequately known lek-formingspecies share many basic similaritiesin their social CATEGORY I: PROMISCUOUS SPECIES THAT FORM organization(Hjorth, 1970; Wiley, 1973a). Dis- LEKS playingmales aggregate for several hours each Sage Grouse, Centrocercus urophasianus(NA)b morningand evening,and sometimesall night, Black Grouse, Lyrurustetrix (EA) at communal displaygrounds, also called arenas aCaucasian Black Grouse, or leks. These aggregations recur from year Lyrurusmlokosiewiczi (A) to yearat the same traditionallocations. Females Greater Prairie Chicken, come there to mate, although at least in some Tympanuchuscupido (NA) of the species a small fractionof the copulations aLesser Prairie Chicken, are performed by solitarymales (Hamerstrom Tympanuchuspallidicinctus and Hamerstrom, 1960; Hjorth, 1970; Kruijt, (NA) de Vos, and Bossema, 1972). The period of Sharp-tailed Grouse, Pedioecetes two or three weeks during which females visit phasianellus(NA) Capercaillie, Tetraourogallus a lek is considerably shorter than the period (EA) of severalmonths during which the males attend aSmall-billed Capercaillie, Tetrao regularly. Males make no contribution to parvirostris(A) parental care. CATEGORY II: PROMISCUOUS SPECIES WITH Within each lek, individual males occupy DISPERSED MALES territoriesdemarcated by boundary zones in Blue Grouse, Dendragapus whichneighbors encounter each other.The size obscurus(NA) of the males' territoriesand the degree to which Spruce Grouse, Canachites males intrude into neighbors' territoriesvary canadensis(NA) with the species and with the presence or aSharp-winged Grouse, Falcipennisfalcipennis (A) absence of femaleson the lek. Male Sage Grouse Ruffed Grouse, Bonasa umbellus and Black Grouse usuallyremain withinor near (NA) theirboundaries even when femalesare present CATEGORY III: SPECIES THAT FORM PAIR-BONDS elsewhereon thelek (Wiley,1973a; H6hn, 1953; Hazel Grouse, Tetrastesbonasia Kruijt and Hogan, 1967; Kruijt, de Vos, and (EA) Bossema, 1972). Male Greater Prairie Chickens aAmur Grouse, Tetrastes and Capercaillie,on the otherhand, oftenleave sewerzowi(A) theirterritories to approach females elsewhere White-tailedPtarmigan, Lagopus on the lek, although when females are absent leucurus(NA) they remain withinnearly exclusive territories Rock Ptarmigan,Lagopus mutus (NA, EA) (Hamerstrom and Hamerstrom, 1960; Robel, Willow Ptarmigan,Lagopus 1964; Lumsden, 1961; Hjorth, 1970). lagopus(Red Grouse, L. 1. Most copulations are performed near the scoticus)(NA, EA) center of the lek by a minorityof the attending aSpecies whose behavior remains largelyunknown. males (Schwartz, 1945; Lumsden, 1965; Kruijt Available evidence suggeststhat in theirsocial behav- and Hogan, 1967; Koivisto, 1965; Wiley, ior they resemble their nearest relatives (Dementiev 1973a). Only a few studies have estimated the and Gladkov, 1967; Hjorth, 1970). distributionof matings among the males at- bApproximate distribution within the Holarctic tending a lek. In his studies of Black Grouse, region: NA, North America; EA, Europe and Asia; Koivisto (1965) reported that one male on a A, Asia. lek attended by ten males performed nearly three-quartersof the copulations observed (17 of 24). One-third of the males performed 75 ments to a common area. In such situations, per cent of the matingsobserved by Kruijt and a full understanding of heterosexual relation- Hogan (1967) during two years on one lek. ships would require intensive studies and ex- On three Sage Grouse leks, about 10 per cent perimentation. of the males performed 75 per cent of the 204 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49 copulations (Wiley, 1973a). A three-yearstudy priate a vacancy near the center of a lek or at one Sage Grouse lek also revealed that only even expel the original resident(Hjorth, 1970; a fewmales performeda preponderantmajority Kruijt, de Vos, and Bossema, 1972; Hartzler, of the copulations (Hartzler, 1972). The Sage 1972). Grouse is possibly the most polygynousof all In all lek-forminggrouse, year-old males birds. attend leks less constantlythan do older males. Females apparently visit one or a few leks They establish territorieson leks later in the on several morningsbefore copulating,at least season and then occupy peripheral positions in Sage Grouse (Lumsden, 1968), Greater (Lack, 1939; Lumsden, 1965; Koivisto, 1965; Prairie Chickens (Hamerstrom and Hamer- Kruijt and Hogan, 1967; Robel, 1967; Patter- strom,1955; Robel, Briggs,Cebula, Silvy,Viers, son, 1952; Wiley, 1973a). Some young males and Watt, 1970) and Black Grouse (Kruijt, de never become territorial(Black Grouse: Robel, Vos, and Bossema, 1972). The numberof times 1969). Owing in partto theirlater establishment a female mates each season is unclear. In Sage and peripheral positions,year-old males almost Grouse the available evidence indicates that never copulate. Hjorth (1970), however, did females need to copulate only once in order observe a number of copulations by first-year to lay a fertileclutch and that females normally male Sharp-tailed Grouse when one of the mate only once or perhaps a few times each older, central males failed to return after he season (reviewed in Wiley, 1973a). Whether or was trapped. not females develop preferencesfor particular In first-yearmale Sage Grouse, and probably males, particularleks, or particularsites within in other lek-formingspecies as well, growth leks remains uncertain (see below, Female of the testesis delayed in comparison withthat Choice). The behavior of first-yearand older of older males, and the average testis weight females might differsignificantly in these re- never reaches the average for older males at spects. the peak of the mating season. Year-old males Females evidently normally breed in their do, however,produce spermatozoa (Eng, 1963). firstspring (Dalke, Pyrah, Stanton, Crawford, In several lek-formingspecies year-old males and Schlatterer,1963). There are some sugges- have noticeably less well-developed plumage tions that in Sage Grouse year-old females than do older males. The tail feathers, an ovulate on the average a week or two later than importantcomponent of theirdisplay postures, older females (Dalke et al., 1963). are often shorter and less distinctivelydevel- Studies of permanentlymarked males have oped (Sage Grouse: Patterson,1952; Eng, 1963; shown that they tend to return to the same Wiley, 1973a,b; Black Grouse and Capercaillie: lek in successiveyears and to occupy territories Fuschlberger, 1956). Males of the latter two at or near the same sites withina lek (Greater species are also browner and less iridescentin Prairie Chickens: Hamerstrom and Hamer- their firstyear. Male Caucasian Black Grouse strom, 1960; Robel, 1967; Black Grouse: Koi- retaina relativelyfemale-like plumage through visto, 1965; Hjorth, 1970; Kruijt, de Vos, and theirfirst year (Dementiev and Gladkov, 1967), Bossema, 1972; Sharp-tailed Grouse: Evans, an extreme example of a trend apparent in 1969; Sage Grouse: Hartzler, 1972). Territorial the other lek-formingspecies. Acoustic signals positions do change, usually when a male that are characteristicof behavior on leks also occupies part or all of an adjacent vacancy, differsomewhat in first-yearand older males both within a season and from year to year. (Wiley,1973b; Fuschlberger,1956). In general, These shifts often bring the territorialmale then, year-old males among the lek-forming closer to the center of the lek (Evans, 1969; species lag behind older males in theirphysiolo- Wiley, 1973a; Kruijt, de Vos, and Bossema, gical maturation,manifest somewhat less well- 1972). However, this centripetal tendency in developed plumage and displays, and seldom, territorialshifts is not invariable(Kruijt, de Vos, if ever, copulate. and Bossema, 1972; Hartzler, 1972). Although vacanciesoccurring during thebreeding season, at least in Sage Grouse and Black Grouse, are A Variant Among Lek-FormingGrouse usually occupied by males with contiguous territories,on occasion a newcomerwill appro- The Capercaillie, as Hjorth (1970) indicates, SEPTEMBER 1974] EVOLUTION AMONG GROUSE 205 is the mostdivergent of the lek-formingspecies. PromiscuousSpecies with Displaying Males Hjorth even suggests that their aggregations WidelyDispersed (Category II) are not appropriately termed leks. However, the differenceslie primarilyin the large terri- In three species of grouse (Blue, Ruffed,and tories of the males and the small number of Spruce), the males display at widely separated males on most leks. The displayingmales defi- sites, yet the sexes apparently do not form nitely congregate, except perhaps in regions durable pair-bonds. Most reports of these spe- of verylow population density.This clustering cies suggest that the males and females do not remains apparent ih spite of the males' large remain togetherfor an appreciable time at any territories. stage of the breeding cycle. The movements Where theterritories of twoneighbors adjoin, of female Blue Grouse and RuffedGrouse, for the boundary zone is wide, perhaps 20 to 50 instance,are not confined to the vicinityof any meters across in most cases (Lumsden, 1961). one male (Bendell, 1955a; Bendell and Elliott, In relation to the diameters of their territories 1967; Brander, 1967). Boag (1966) found that (about 100 meters),however, the widthsof these female Blue Grouse occupy overlapping home boundary zones seem hardly greater than in ranges, which are much larger than the terri- Sage Grouse (Wiley, 1973a). Boundary encoun- toriesof individual males. However, Blackford ters between neighbors are less frequent than (1963) reportedan associationbetween one pair in otherlek-forming species but are oftensevere of Blue Grouse, although the female often left and protracted(Hjorth, 1970). When females the male's territory.This case might represent visitthe lek, the males often desert their terri- an apparent bond that resulted from the two tories to approach the females, behavior that individuals'attachments to an overlappingarea. recallsthat of the Greater Prairie Chicken. One Female Spruce Grouse choose somewhat more limited study has indicated that, of the adult open habitatfor nestingthan do the males for males in one aggregation,a minorityperformed display posts (Ellison, 1971). As a result, the most of the copulations (Lumsden, 1961). femalesoften nest at a distance fromthe males' The Capercaillie's social organizationon the stations,a situationthat indicates only transitory ground, then, aside from being more spread relationshipsbetween the sexes. Heterosexual out,resembles that of otherlek-forming grouse. associations in these species thus seem nearly In theirforested habitat, male Capercaillie dis- as transitoryas in the lek-formingspecies. play from arboreal sites as well. Each male Displayingmale Blue Grouse, RuffedGrouse Capercaillie usually performs from a specific (Bump, Darrow, Edminster,and Crissey,1947; tree in the evening and again early in the Gullion, King, and Marshall, 1962; Gullion, morning, before he begins to display nearby 1967), and Spruce Grouse (MacDonald, 1968; on the ground (Fuschlberger, 1956; Hjorth, Ellison, 1971) disperse themselvesmore or less 1970). These trees used for "Hochbalz" and evenly throughout the suitable habitat. In all for roostingare often more dispersed than the threespecies males withestablished display sites positions occupied during terrestrialdisplay produce long-range acoustic signals. Gullion ("Bodenbalz") (Hjorth, 1970), so aggregation (1967) noted, without quantification,a slight of males is less pronounced in the former. In clusteringof Ruffed Grouse display sites, but their arboreal behavior male Capercaillie ap- it is not clear from his account whether this proach those species in which displayingmales clustering is explained by the males' habitat have widely dispersed stations (Category II, preferences. By challenging or attacking in- below); however, even in arboreal display, the truders,male Blue Grouse defend nearlyexclu- males formaggregations. sive territories,averaging 4 hectares or more As in the other lek-formingspecies, year-old around their display sites (Blackford, 1963; male Capercaillies begin to display later in the Boag, 1966; Bendell and Elliott, 1967). In spring than do older males and they occupy contrast, resident male Ruffed Grouse and peripheral positions on the leks. Indeed, Kiri- Spruce Grouse occupy areas without definite, kov (cited in Dementiev and Gladkov, 1967) defended boundaries. Male Spruce Grouse concluded that even two-year-oldmales were neverthelessreact quicklywhen theydetect the later than older males in their seasonal onset presence of nearbyconspecific males (MacDon- of display. ald, 1968). Male RuffedGrouse willuse tempo- 206 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49 rary display sites to approach neighbors who a minorityof the display sites are reoccupied are displaying nearby, but overt aggression is in the same season, but the newcomers again virtuallynever reported (Gullion, 1967). The are usually first-yearmales (Dorney and Kabat, dispersion of displaying males distinguishes 1960). The mechanisms underlying the reoc- these species from the lek-forming grouse. cupation of vacancies remain unclear. In no Although three males whose territories or study so far have the newcomers' previous ranges adjoin at a common point might occa- locations been known in detail. Nor has any sionallyapproach each other, in none of these studycompared vacancies created early in the species do displayingmales regularlyaggregate season, prior to most of the mating,and vacan- in the clear way that even male Capercaillie cies created later, afterthe mating. regularlydo. Nothing is known about the distributionof Once a male Blue Grouse has established a matingsamong the males of CategoryII species, territory,he normallyreturns to that territory owing to the difficultiesof observing widely in successive seasons as long as he survives dispersed birds in forestedhabitats. It remains (Bendell and Elliott, 1966, 1967). Male Ruffed unknownwhether sites occupied by a succession Grouse, on the other hand, often change their of males offeradvantages in attractingfemales, display posts if they survive several years, but and whether females develop preferences for the factors that influence the coice of a new mating with particular males or at particular site remain unknown (Gullion, 1967). sites. Many male Blue Grouse in their firstyear Both in Blue Grouse and in Ruffed Grouse, do not establishdisplay territories(Bendell and most females breed in theirfirst year (Bendell Elliott, 1967). These unestablished yearlings and Elliott, 1967; Zwickel and Bendell, 1967; remain silentand move around widely. In this Bump et al., 1947). On the other hand, in all species first-yearmales have smaller testes, three species many first-yearmales evidently shorter tails, and weigh less than older birds do not mate, to judge from their less well- (Bendell, 1955b; Bendell and Elliott, 1967; developed territorialbehavior, less persistence Swarth, 1926). Bendell and Elliott (1967) have in displaying,and, at least among Blue Grouse, suggested that resident male Blue Grouse at- smallertestes and somewhatless well-developed tractunestablished year-old males to theirterri- plumage. If most first-yearfemales do mate, tories.These yearlingssometimes occupy these while year-old males usually do not, and pro- sitesif the usual occupant is removed. Resident vided that the mortalityof females is not much Ruffed Grouse and Spruce Grouse also seem greater than males (see below), then polygyny to attractfirst-year males (Gullion, 1967; Elli- is the probable result. son, 1971). Often a year-old male Ruffed Grouse regularly frequents the vicintyof an- SpeciesThat FormPersistent Pair-Bonds other male's display site, yet rarely displays. (CategoryIII) Marshall (1965) and Gullion (1967) have noted thaton severaloccasions when the residentmale The only grouse that normallyform durable had disappeared, such a yearlingoccupied the pair-bonds are the three species of ptarmigan vacated display site. In this way some display (Lagopus) and the Hazel Grouse (Tetrastesbona- sites are used by a succession of males, so that sia). Of these, the Red Grouse (L. lagopus the locations of these sites become traditional. scoticus),an insular race of a widespread arctic The experimentalremoval of residentmales and subarcticspecies, is by far the best known. in both of these species allows some first-year Male Red Grouse establish territoriesin au- males to establishthemselves in thevacated sites, tumn, but these territories,several hectares in but many vacancies remain unoccupied at least area, are not intensivelydefended until the until the following year. When Bendell and followingFebruary. Hens associate withterrito- Elliott (1967) removed from their territories rial males during the autumn and winter,but 31 male Blue Grouse, less than a thirdof which theyoften move fromone male to another until were yearlings,two-thirds of the new occupants pair-bondsare firmlyestablished in earlyspring were first-yearmales. Eighteen of the vacated (Watson and Jenkins,1964). Males intrudeinto territories(58%) remained unoccupied. If resi- theirneighbors' territories in pursuitof a female dent male Ruffed Grouse are removed, only or when the resident male is occupied at a SEPTEMBER 1974] EVOLUTION AMONG GROUSE 207

distance. When challenged, however, the in- their firstyear is about equal to that of older trudernormally retreats within his own bound- males. Consequently,first-year and older males ary. Confrontationsof neighboring males de- would seem to have about the same chances fine relativelynarrow boundary zones between of establishingterritories. their territories(Jenkins, Watson, and Miller, The resultsof removal experimentssuggest, 1963). on the other hand, thatolder males mighthave The behaviorof male and femaleRed Grouse some advantages in the establishment of a gradually changes as the pair-bond is formed. territory.When Watson and Jenkins (1968) The male becomes less aggressive,and concur- removed territorialRed Grouse during early rentlythe female's tendency to avoid him de- autumn (August and September), before first- creases. Eventually,during the period before year males normallyestablish territoriesin un- incubation,the male closelyfollows the female's disturbed populations, most of the vacancies movements. The female, in turn, sometimes were filledwithin a few days by yearlingmales lures her mate away fromother nearbyfemales. only a fewmonths old. Thus, in the early stages During incubationthe hen oftenjoins her mate of territoryestablishment, the presence of older during her periods off the nest. Afterthe eggs males seems to prevent territorialbehavior in hatch both parents attend the brood (Nether- yearlings. Vacancies created from November sole-Thompson and Nethersole-Thompson, throughJune sometimesremained unoccupied 1939; Jenkins,Watson, and Miller, 1963; Wat- for weeks or months.The eventual newcomers son and Jenkins, 1964; also other subspecies during these months included about equal of L. lagopus:Swarth, 1926; Dixon, 1927; Rajala, numbers of first-yearmales without previous 1962; Weeden, 1965b; Dementievand Gladkov, territoriesand older males that moved their 1967). Both sexes attack predators near the territoriesinto the vacancies, in one case from brood or the nest, or lure them away, often a distance of one kilometer.A few older males by feigning injury. In addition, males lure that had previouslylacked territoriesalso took potential predators away from their mates positions in the vacancies. (Nethersole-Thompson and Nethersole- By mid-winter,then, all but a fewolder males Thompson, 1939; Watson and Jenkins,1964). have either established territoriesor have be- Red Grouse broods often,although not invaria- come permanentlynon-territorial; perhaps they bly, remain withinthe male's territoryfor sev- have died or emigrated. It appears that some eral months after hatching (Jenkins,Watson, first-yearmales, however, are stillexcluded by and Miller, 1963), though in other populations previously established birds. The fraction of broods mightprove less sedentary.Paired Red spring territoriesoccupied by year-old males Grouse thus maintain their association for and the interactions between first-yearand nearly six monthseach year. older males during territoryestablishment have A small fractionof the territorialmale Red yet to be reported. Grouse mate with two females, while a few Rock and White-tailedPtarmigan also nor- territorialmales remain unmated. Bigamous mallyform monogamous pairs, whichmaintain males usually devote more attentionto one of large territories.Like Red Grouse, two females theirmates (Watson and Jenkins,1964). Those will occasionally settle in one male's territory, males that fail to attract a mate often have in which case the male tends to favor one of smaller than average territories. them (MacDonald, 1970). In these species, Many male Red Grouse establish territories though,the association of the mated pair usually and breed successfullyin their firstyear, al- ends duringincubation or shortlyafter hatching though older males become territorialone to (Swarth, 1926; Choate, 1963; Watson, 1965, twomonths earlier in autumn (Jenkins,Watson, 1972; Weeden, 1965a,b; Dementiev and Glad- and Miller, 1963; Watson, 1967). Whether this kov, 1967; MacDonald, 1970). Male Rock lead gives older males an advantage over first- Ptarmigan in some arctic regions leave the year males in establishingterritories is unclear. nesting region altogether, in order to molt On one hand, Jenkins,Watson, and Miller, (Semenov-Tyan-Shanskii,1960). The pair-bond (1963, 1967) deduce that territorialbirds sur- can terminate even sooner, at the start of vive much betterthan non-territorialbirds and incubation.Female White-tailedPtarmigan, for that August to August survivalof males during instance, sometimes nest outside their mate's 208 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49

territory,in one case at a distanceof 400 meters, flockingappear in a number of species (Wee- so that in this case the female terminated the den, 1964; Seiskari, 1962), and studies of other pair's association (Choate, 1963). species might uncover similar tendencies. Al- Some male Rock Ptarmigan do accompany though our informationon winterbehavior is broods and help to distractpredators (Parmelee, stilllimited, one is struckby a similarityamong Stephens, and Schmidt, 1967; Watson, 1972). species that contrastswith the diversityin their Usually, however,only females feign injury or mating behavior. otherwise defend the brood from potential predators (MacDonald, 1970). Males regularly performthese activitiesonly while the female Gradationswithin the Proposed Classification is incubating (Watson, 1972). In an alpine population in Scotland, females with broods Although I have presented the-socialsystems oftenremained withintheir mate's formerter- of grouse during the breeding season in three ritory(Watson, 1965), but in arctic populations categories,variations within the categories sug- broods tend to move widely (Weeden, 1965a; gestthat they actually intergrade. The enduring MacDonald, 1970). pair-bond of the Red Grouse, and presumably First-year male White-tailed Ptarmigan other subspecies of Willow Ptarmigan, clearly usually arrive on the breeding grounds later is one extreme in grouse social organization. than older males and are less successful in In other ptarmiganand the Hazel Grouse, the establishingterritories. The one available study association of the sexes, although lasting a suggeststhat when theydo establishterritories, number of weeks, usually soon ends once in- these tend to be smaller,and theirchances for cubation begins. Among the four species in successful mating are low (Choate, 1963). Al- Category II interactionsof the sexes prove still though Watson (1965) did not differentiate more evanescent. Pair-bonds probably vary first-yearmales, males that displayed less per- somewhat among individuals and perhaps sistentlyand had smaller territorieswere less among populations of the same species. successful in attractingmates. By comparison CategoriesII and III probablyalso intergrade with Choate's (1963) studies of banded White- in the roles taken by first-yearmales and in tailed Ptarmigan,it seems possible that many breeding sex ratios.While many first-yearmale of Watson'sless successfulmales were yearlings. Red Grouse breed successfully,first-year male Territorialityand heterosexual associations White-tailedPtarmigan, according to the one in Hazel Grouse closelyresemble those of Rock report available, were less successfulin attract- and White-tailed Ptarmigan. Males establish ing mates. In their heterosexual relations the territoriesin autumn, but pair-bonds are not difference then between the White-tailed firmlymade until early spring. Males rarely Ptarmigan (Category III) and the Ruffed have more than one mate. Before incubation Grouse (Category II) thus appears to lie in the begins, the pair clearlycoordinate theirbehav- longer association of male and female ptarmi- ior, by calling back and forth to each other, gan prior to copulation. forinstance, but the associationdoes not usually Categories I and II are probably similar in persist through incubation. Males usually do their heterosexual relations. However, our not accompany broods; apparently only the knowledge of the interactionsbetween identi- female feigns injury to protect the brood fied individuals of both sexes is insufficientto (Pynn6nen, 1954; Fuschlberger,1956; Demen- allow firmconclusions. Perhaps when males are tiev and Gladkov, 1967). Occasional reports of widelydispersed there are greateropportunities males with broods might result from chance for longer and more intricate relationships occurrence or from some individual variation between individuals of opposite sex. in male behavior. Directevidence is lacking for the distribution of matingsamong individualmales of the Cate- WinterBehavior gory II species. For this reason, it remains unclear how the species in Categories I and During the wintermost grouse form flocks, II compare in theirdegree of polygyny.Breed- which sometimes include large numbers of ing sex ratios might well vary among popula- individuals. Tendencies toward unisexual tions or years in the same species. SEPTEMBER 1974] EVOLUTION AMONG GROUSE 209

Promiscuity,Polygyny, Male Dispersion, and Male of the greatest risks in parental care probably Parental Care accompany the parent's attempts to deflect predators fromthe nest or young. The aggregation or dispersion of displaying Only in the Willow Ptarmigandoes the male males clearlyhas no necessaryconnection with normally aid in guarding the brood from promiscuity(Hjorth, 1970; Selander, 1972). predators. His attentivenessnear the nest dur- Although the species in Categories I and II ing incubation might, in addition, reduce a are all promiscuous, the two categories differ predator'schances of surprisingand killingthe in the dispersionof displayingmales. All grouse female on her nest. In the other two species that form pair-bonds also manifest dispersed of ptarmigan and the Hazel Grouse, although territoriality. all form stable pair associationsbefore nesting Polygyny probably always accompanies begins, the bond usually terminates during promiscuityamong the grouse. The evidence incubation.Among grouse, then, reduced male for this point will remain incomplete until we parental care is not restrictedto species with have direct estimatesof breeding sex ratios for promiscuous or polygynoussexual relations. Category II species. Our present knowledge In conclusion,the radiationof tetraonidsocial of the behavior of year-old males and of mor- organizationhas involved at least three dimen- talityrates in these species, however, suggests sions: the dispersion of displaying males; the that they are indeed polygynous (see above). breeding sex ratio; and the male's contribution If this conclusion is correct, all promiscuous to parental care. grouse are polygynousto varyingdegrees, while all grouse that form pair-bonds are normally monogamous. CORRELATES OF SOCIAL STRUCTURE AMONG GROUSE A third feature of social organization, the The followingsections will review evidence reduction of male parental care, is associated thatreproduction by year-oldmales, overall size withboth monogamous and polygynousmating as indicated by female weight, sexual dimor- systems(Table 2). All polygynous,promiscuous phism in weight,and habitatstructure all corre- species lack male parental care. Among species late in some degree with social structure.On that form monogamous pair-bonds, however, the otherhand, available evidence suggestslittle the males varyin theircontributions to parental association between variationsin social organi- care. In all grouse the female alone incubates zation in grouse and theirdiets, mortality rates, the eggs. The precocial young are not fed by or clutch sizes. their parents, although the mother helps by leading her chicksto appropriate feeding areas and by directingtheir attention to food items. A parent, in addition, contributessubstantially Reproductionby Year-old Males to the securityof the brood. For grouse some The preceding review of tetraonid social systemshas already documented one striking TABLE 2 correlate of social organization: in polygynous Parentalcare bymale grousein differentsocial systems species first-yearmales generallydo not breed, although year-old females do (Table 3). This correlation recurs in other groups of birds, TYPE OF INCIDENCE OF PARENTAL CARE BY MALES and SOCIAL OCCAStON- notablythe Ploceidae (Crook, 1964) Icteri- SYSTEM NEVER ALLY USUALLY dae (Selander, 1965, 1972). Furthermore,sex- Category I Centrocercus ual differencesin the age at onset of reproduc- Tympanuchus tionalso characterizepolygynous mammals (see, Pedioecetes for instance, Carrick, Csordas, Ingham, and Lyrurus Keith, 1962; Geist,1968a,b; McCullough, 1969). Tetrao The association of polygynywith deferred Category II Dendragapus reproductionin male grouse seems to be consis- Bonasa tent.In the most polygynous,lek-forming spe- Category III L. mutus L. lagopus cies, such as the Sage Grouse, first-yearmales Tetrastes essentiallynever breed. In the species that form 210 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49

TABLE 3 1967; Robel, 1967; Kruijt,de Vos, and Bossema, 1972). Breedingby first-year male grouse in differentsocial systems At least in Blue Grouse and Sage Grouse year-old males have smaller testes on the INCIDENCE OF BREEDING BY average than older males. Also their testicular TYPE OF FIRST-YEAR MALES SOCIAL NEVER, OR OCCASION- growth is delayed in comparison with older SYSTEM RARELY ALLY USUALLY males, although first-yearmales of both species CategoryI Centrocercus produce spermatozoa (see above; Bendell, Tympanuchus 1955a; Eng, 1963; Bendell and Elliott, 1967). Pedioecetes Although other species of grouse have not yet Lyrurus been investigatedin thisregard, two polygynous Tetrao icterids, the Red-winged Blackbird Agelaius CategoryII Dendragapusa phoeniceusand the Great-tailedGrackle Quisca- Bonasaa lus mexicanus,also show age-related differences CategoryIII L. leucurus L. lagopus in testiculargrowth (Wright and Wright,1944; L. mutus Selander and Hauser, 1965; Selander, 1972). a Someyear-old males establish territories or display Deferred reproduction by first-yearmales of sitesbut their breeding status remains unknown. polygynousbirds is thus associated withretard- ed maturationof the gonads. The term sexual smaller leks, such as the Sharp-tailed Grouse, bimaturismis appropriate to describe a substan- year-old males are occasionally reported to tial difference between the sexes in the age copulate, but normallythey do not. at which adult reproductive physiologyis at- Among the Category II species, some first- tained. year males establishterritories, but mostdo not. However, it remains uncertain whether even Weightof Femaleand Sexual Dimorphismin territorialyearlings mate successfully.Among Weight the species that form pair-bonds, the most persistentheterosexual affiliation occurs in that Polygamous,sexually dimorphic species often species, the Willow Ptarmigan,in which first- tend to be larger than related monogamous year males normallybreed. In the other two species (Amadon, 1959; Selander, 1972). This species of ptarmigan,both of whichhave briefer relationship applies with a few exceptions to pair associations,first-year males seem less likely the grouse. A strikingcorrelation also pertains to breed successfully,and the incidence of between the degree of sexual dimorphism in polygynous relationships seems somewhat weight and the overall size of a species, as higher. indicated by the average female weight. Females in all species of grouse normallydo The ratio of male to female weightsincreases breed in their first year. Thus in males of almost linearlywith increases in female weight polygynousspecies the age at firstreproduction (Fig. 1). Informationon the weightsof grouse, is later than in females and is later than in it should be noted, includes many uncertainties. males of related monogamous species. Weightsvary somewhat fromseason to season, It remains uncertainwhether mating success from year to year, and from place to place among males of polygynous species increases even within relativelylimited regions (Koski- with age even beyond their firstyear, though mies, 1958), and the weights of only a few indirectevidence suggests that.thismay be so species have receivedcareful study.I have used in Sage Grouse (Wiley, 1973a). Unlike year-old published means from samples of at least five males, some two-year-oldsdefinitely do copu- weights for each sex. All these weights were late (Hartzler, 1972), but it still is not known obtained during summer and autumn, or at how theirmean frequencyof mating compares unspecifiedtimes of year. If wing lengthis used withthat of older males. There are also sugges- as a measure of size, instead of weight (see tions of age-correlated mating success beyond Amadon, 1943), the correlation of sexual di- the firstyear among male Black Grouse, Caper- morphism in size with female size remains caillie, and Greater Prairie Chickens (Koivisto, virtuallythe same. 1965; Kirikov,cited in Dementievand Gladkov, Within the Tetraonidae sexual dimorphism SEPTEMBER 1974] EVOLUTION AMONG GROUSE 211

2 5- species are about the size of female ptarmigan, which form monogamous pair-bonds. If the Ruffed Grouse is instead compared with its approximate ecological counterpartin the Old E World, the Hazel Grouse, the promiscuous L 20- species is then both larger overall and more Cu Cu> dimorphic in weight than the pair-bonding species. Promiscuityamong grouse is thus related not only to increased sexual dimorphism CN_ but also to increased size of the species. This X 15 triple relationship holds both for the forest Dk species and for the open-countryones.

? TC,\

LMN - Habitat Preferences cc. \LL TB 10- Differences in social organization among

0 05 1.0 15 20 grouse show one clear association with dif- Average Female Weight (kg) ferences in habitat type: promiscuous species in open habitats form leks, while the males of most promiscuous species in forested habitats FIG. 1. RELATIONSHIP BETWEEN OVERALL SIZE, AS remain dispersed. The promiscuous species are INDICATED BY FEMALE WEIGHT, AND SEXUAL almostevenly divided betweenopen and forest- DIMORPHISM IN WEIGHT AMONG THE SPECIES OF GROUSE Each point presentsthe average female weightand ed habitatsin the temperatezone. Those species the ratio of average female weight to average male that formleks (Category I), however,all occur weightfor one published sample. Solid lines connect in open habitats, with the exception of the twoor more publishedsamples forone species. Letters Capercaillie, a denizen of mature coniferous identifythe pertinentspecies: TU, Tetrao urogallus; forests.The Black Grouse favorsan intersper- CU, Centrocercusurophasianus; D, Dendragapus ob- sion of forest and open areas, often moor or scurus;LT, Lyrurustetrix; TC, Tympanuchuscupido; steppe. Their leks, though,are generallyin the P, Pedioecetesphasianellus; B, Bonasa umbellus;CC, open. In contrast,those species in which males Canachitescanadensis; LL, Lagopus lagopus; LM, L. take dispersed positions (Category II) occur mutus;TB, Tetrastesbonasia. primarilyin forests.Thus among promiscuous grouse,the habitat has a more definiteinfluence in weight provides a good discriminant for on the dispersion of displaying males than on differences in mating systems. The Hazel the breeding sex ratio. Grouse and the ptarmigans,species that form In habitatswith restrictedvisibility, the risks pair-bonds,have the lowestsexual dimorphism. of predation on a congregationof grouse could Among the lek-forming species, the Sage militateagainst the evolution of leks. The fact Grouse, which forms the largest leks, has the that only Capercaillie form leks in forests is second highest discrepancyin weight between perhaps the exception that proves the point. the sexes. The species that form smaller leks Of all grouse the Capercaillie, owing to its large in open country have less dimorphism. This size, should have the fewestpotential predators. relationshipsuggests that among promiscuous Although they are the only forest grouse to species the more polygynousones are also more formleks, male Capercaillie keep fartherapart dimorphic in size. Full evaluation of this sug- than the males of any otherlek-forming grouse. gestionis impossible until the degree of polyg- The few monogamous species occupy a great ynyamong Category II species and Capercail- diversityof vegetationformations. Particularly lie is betterknown. catholic in habitat preferencesare the various Average female weight can also serve to subspecies of the Willow Ptarmigan. The race discriminatedifferences in matingsystems. The endemic in the British Isles, L. 1. scoticus, promiscuous species are larger as well as more occupies open moors, a habitat as exposed as dimorphic,except for the Ruffed and Spruce the steppes and prairies of western North Grouse. The females of these two promiscuous America. Another subspecies of the Willow 212 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49

Ptarmigan,L. 1.major, ranges along the interface trespassed on territoriesin optimal habitat in between steppe and deciduous forestin central order to feed there (Moss, 1972). Here the Asia (Dementiev and Gladkov, 1967), a situation failure of a female to restricther movements favored by several races of the Sharp-tailed to her mate's territoryevidently does not pre- Grouse in North America. Most populations clude pair-bonding. Hazel Grouse and Ruffed of the Willow Ptarmigan, however, occur in Grouse occupy similarhabitats and presumably the shrubby tundra near or beyond the tree experience similarlydispersed food supplies, line. The Hazel Grouse occupies a varietyof but they differappreciably in their social be- relatively mature forest types, deciduous, havior. mixed, and coniferous, across the breadth of Among the grouse withdispersed males and Eurasia. promiscuous sexual relations (Category II), female movements prior to egg-layingare nor- Food Habits mally not restrictedto any one male's territory All grouse are primarily herbivorous, al- (see above). To decide whether this tendency though all probably eat considerable numbers is a cause or a consequence of promiscuitywould of insects during the summer months. The require careful analysis. For instance,although chicks of all species seem to take many insects female Ruffed Grouse wander widely with re- in theirdiets. Thus, in contrastto the remarka- spect to the males' stations,such large, widely ble divergencein theirsocial organization,their overlapping ranges might arise either because food habits are basicallysimilar. There are no the females have no attachmentsto individual gross differences in diet correlated with dif- males or because no smallerarea would include ferencesin social structure,as there are among adequate food resources. When food supplies the Ploceidae, for instance (Crook, 1962). are uniformlydistributed, females could pre- Species and populations of grouse do differ sumably find as much food on larger, more in the diversityof theirdiets and the uniformity overlapping ranges as they could on smaller, of the dispersion of their food plants. Kruijt, more exclusive ranges. The evolution of large de Vos, and Bossema (1972) have related the male territoriesin grouse and the restriction differencesin the social structureof Red Grouse of females' movementsto these territoriesevi- and Black Grouse to differencesin the variety dently requires both a uniformlydistributed and dispersionof theirfoods. The Red Grouse food supplyand monogamy.A uniformdisper- subsistsprimarily on the leaves and shoots of sion of food,resources seems necessary,but not one plant, Calluna vulgaris,which is dominant sufficient,for the evolution of large male terri- over large areas. Female Black Grouse preced- tories in grouse. ing and during egg-layinghave a more diverse The effectsof food dispersion on the move- diet and range over a larger area. Kruijt, de ments of individuals thus seem not to explain Vos, and Bossema (1972) point out that only the evolution of grouse social structure.The when food is more or less uniformlydistributed effectsof food dispersion on social structure, can a male efficientlydefend a territorylarge however,do not necessarilyact directlythrough enough to supply his mate's nutritionalrequire- effectson the movementsof individuals.A later ments (see Brown, 1964). section will discuss the relations among social Among grouse, however, uniformlydistrib- structure,sexual bimaturism,and body size in uted food resources are not always associated grouse and willraise the possibilitythat a species' withlarge male territoriesor monogamy. The food supply might affect its social structure Sage Grouse (Category I), in particular, con- more indirectly,through an effecton the evolu- sumes little except the leaves of one species tion of its body size. Elucidation of the relation- of plant, Artemisiatridentata, which is the domi- ship between feeding strategies and social nant plant in the Sage Grouse's habitat. Nor structurein grouse willprobably require a more do more diverse diets and less uniformlydis- exact knowledge of feeding strategiesand food persed food always imply promiscuityand ab- dispersion than is now available. sence of large male territories.Populations of the Willow Ptarmigan other than the Red MortalityRates and ClutchSizes Grouse consume twigs,buds, leaves, and catkins froma varietyof shrubbyplants. In a population Mortalityrates and clutchsizes varyconsider- in Alaska, pairs with territoriesin poor habitat ably from population to population and from SEPTEMBER 1974] EVOLUTION AMONG GROUSE 213 year to year withinany one species. Differences Once males are liberated from parental duties, among the species are generally not apparent competition among them will restrictmating from the evidence now available, and no cor- opportunities to a minority (see Armstrong, relationswith social systemsare evident. Mea- 1955; Crook, 1962, 1964; D. Snow, 1963; Lack, surementsof adult mortalityrates have ranged 1968). from 25 per cent to 80 per cent per year (see According to this theory, polygynyshould Wiley,1973a; also Robel, Henderson, and Jack- evolve frequentlyin species whose food supply son, 1972). Several comparisons of mortality during the breeding season is so abundant that rates in the second and later years of life have one parent can feed the young nearly as suc- suggested that mortalityrates remain constant cessfullyas two. The rate at which a parent afterthe first year. Three reportson twospecies, can supply food, for a given investmentof time the Red Grouse and the Blue Grouse, indicated and energy in foraging, will depend both on that thereare no differencesbetween the sexes the rate at which the food supply is generated in mortality(Jenkins, Watson, and Miller, 1967; in the environmentand on the numberof other Bendell and Elliott, 1967; Boag, 1966). Male individualssimultaneously exploiting that same Ruffed Grouse, however, evidently survive supply. Consequently,for food to remain easily slightlybetter than do females (Gullion and available during the breeding season, the den- Marshall,1968). Some limitedevidence suggests sity of hungry nestlings must not rise in that the same holds for male White-tailed proportionto the supply of food to feed them. Ptarmigan(Choate, 1963). These arguments can help explain why po- The only comparison of mortalityrates for lygynyevolves among species with dense but two species in the same region is Helminen's highlyseasonal food sources, like the seed-eat- (1963) reporton Capercaillie and Black Grouse ing ploceine weaver birds of tropical savannas in Finland. The larger species had much lower (Crook, 1962, 1964), an environmentin which mortality,about 40 per cent in comparison with seeds become available in great quantities for roughly80 per cent. that brief period each year during which the Clutch sizes likewisevary considerably within finches breed. With this sudden surge in the a single species, when samples from different food supply, food evidently becomes easily areas or years are compared. The nutritionof available in spite of the increased demand for the femalesin the period precedingand during food during the breeding season. Polygynyalso layingcan affectthe average clutchsize (Jenkins, emerges frequentlyamong tropical fruit-and Watson, and Miller, 1967). For most species nectar-eatingbirds that build open nests (D. the average clutch sizes reported in the litera- Snow, 1962, 1963; B. K. Snow, 1970, 1972). ture fall between 5 and 9 eggs per clutch, and The high mortalitysustained by such nests in usually between 6 and 8. Three species consis- the tropics would favor cryptic nests, small tentlyaverage 11 to 12 eggs per clutch: Greater clutch sizes, and infrequentvisits to feed the Prairie Chicken, Sharp-tailed Grouse, and young. In these circumstances,the density of Ruffed Grouse. Large average clutch sizes thus nestlings and the parental time and energy have no clear relationshipwith habitat or social required to feed them mightremain relatively system. low in relation to the food supply. Long-distanceforaging to feed the nestlings

THEORIES OF THE EVOLUTION OF POLYGYNY could also favor full parental cooperation (Orians, 1969). Thus species thatnest colonially Theories of the adaptedness of polygynous in protected sites, such as isolated trees or mating systems among birds fall into two marshes, at some distance from their source groups. Although they share a number of of food, tend to have less polygynousbreeding features,they may be labeled for convenience sex ratios and more male parental care than the "surplus-food" and the "patchy-environ- do related species thatforage nearer theirnests ment" theories. The surplus-food theory, the (Orians, 1961; Crook, 1962). earlier of the two, proposes that the absence Although two parents could presumably or reductionof male parental care, a prerequi- always provide more food than could one, two sitefor the evolutionof polygyny,should prove might not provide food as efficientlyas one, adaptive only in species that have a superabun- ifthe second parent by his own food comsump- dance of food available to the breeding females. tion sufficientlyreduced the supply of food 214 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49

nearby. In some species polygynymight deci- The patchy-environmenttheory assumes that sivelyincrease the availabilityof food near nests competitionamong males willlimit the number by reducing the number of males foraging of males that can establishterritories in prime there. Under these conditions, it could prove areas. Both theoriesof theevolution of polygyny more efficientfor one parent to feed the young thus directly address the evolution of single on food found nearer the nest than for both parental responsibility and assume that parents to rear the young on food collected competitionamong males willrestrict successful at greater distances. mating to a few as male parental care wanes. The surplus-foodtheory thus focuses on the Certainly,among grouse, the advantages of evolution of single parental care as the critical dual parentalcare seem minimal,owing to their process in the evolution of polygyny.Reduced predominantlyherbivorous diets and precocial male parental care leads to competitionamong young (Orians, 1969). It is not clear, then, why males, which in turn is assumed to generate dual parental care should have greater advan- an unequal distributionof matings and conse- tages forone of the species, the Willow Ptarmi- quently polygyny. gan, than for the others. Furthermore,single The patchy-environmenttheory, like the sur- parental care is not inevitablyassociated with plus-food theory,proposes that polygynywill polygyny,for three species in two genera prac- evolve only when a reduction in parental care tice monogamy although the males rarely con- by the male has minor consequences for the tributeto brood care: Hazel Grouse, Rock and female's nesting success. The patchy-environ- White-tailedPtarmigan. Although the grouse ment theory, however, formulates more pre- are evidentlyall closely related species, many ciselythe conditionsunder which polygynywill of them have evolved polygyny,whereas others evolve, especially for species in which females with reduced male parental care have not. nest within the territoriesof individual males Monogamy with single parental care is also (Verner, 1964; Verner and Willson, 1966; frequentamong the Anatidae and Scolopacidae Orians, 1969, 1972). Polygynyshould evolve (Lack, 1968). onlywhen those femalesmated bigamouslywith The specific features of the patchy-environ- males in prime habitatbreed more successfully, ment theorydo not easily apply to grouse. In in spite of reduced help fromtheir mates, than only three species does a female regularly re- do femalesmated monogamouslyin poor habi- stricther choice of a nest-site to her mate's tat.In optimalareas, any disadvantagesof single territory:Willow Ptarmigan, including Red parentalcare are offsetby the greateravailabil- Grouse; Rock Ptarmigan; and Hazel Grouse. ityof food near the nest. For polygynyto evolve These species are all normally monogamous. according to thismodel, the availabilityof food The patchy-environmenttheory might well ex- must differconsiderably from one male's terri- plain the occasional instancesof bigamyin these tory to another. Such patchy environments species. For mostgrouse, though, the availability apparently often confront insectivorousbirds of food or nest-siteswithin the male's territory nestingin fresh-watermarshes. The availability probably has had littleinfluence on the evolu- of food is again a critical consideration. The tion of polygyny.Although the adaptedness of densityof nestingfemales in optimalareas must single parental care is perhaps necessary for remain low enough to insure a high ratio of the evolution of polygynyamong grouse, it supply to demand for food there. evidentlyis not sufficient. It should be noted that, among birds with nidicolous young, polygynyis often partially SEXUAL BIMATURISM AND THE EVOLUTION OF withmale care and compatible parental (Verner POLYGYNY Willson,1969). When the females mated to one polygynousmale have staggered nestingcycles, The coincidence of polygynywith deferred the male can contributesome time to feeding reproduction among males suggests a second the young of both his mates (Haartman, 1951; contributingadaptation. Selection for sexual Williams, 1952; Lanyon, 1957; Verner, 1964; differences in the age at onset of breeding, Willson, 1966). In these circumstances one provided that females survive about as well as female, usually the first,receives preferential males, would tend to produce unbalanced treatment from the male (Haartman, 1951; breeding sex ratios,and hence polygyny.When Williams, 1952). the consequent polygynyis incompatible with SEPTEMBER 1974] EVOLUTION AMONG GROUSE 215 fully shared parental care, the evolution of et al., 1962; Geist, 1968, 1971). matingsystems would thendepend on a balance Because spermatogenesisin males of polyg- betweenthe adaptive advantages of dual paren- ynous birds can begin well before successful tal care and the adaptive advantages of sexual breeding or full maturity,year-old males prob- bimaturism. ably have the capacity to copulate successfully. The two theoriesreviewed above both accept The testes of younger males, however, do not without much comment the notion that match in size those of older males. At least competitionamong males will inevitablygener- in the lek-forminggrouse, the later and lesser ate polygyny,once the need for male parental growthof the yearlings'testes probably insures care wanes. This assumptionis accepted because that the older males arrive earlier on the leks the evolutionary benefits of multiple mating in the spring and have strongermotivation to have seemed self-evident.Yet, owing to the defend their positions on the lek. The infre- defermentof breeding among males of polygy- quency withwhich younger males mate is thus nous species, the advantages of polygynyto most likely an immediate result both of the males are not so simple. inadequate development of their secondary By delayingreproduction, males considerably sexual characters and of their inadequate mo- jeopardize their rates of reproductiveincrease tivationto defend positions and perform dis- (Birch, 1948; Cole, 1954; Lewontin, 1965) and plays attractiveto females. hence the spread of their genes in the popula- This retarded maturationmight result from tion. Early breeding must thereforehave coun- behavioral subordination of younger males to teractingdisadvantages in order to allow the older males, or it might occur independently evolutionof delayed reproduction(Lack, 1954; of any interactionswith older males. In flocks Williams, 1966a,b; Gadgil and Bossert, 1970). of domesticfowl, full development of the testes Any complete theoryof the evolution of polyg- is inhibitedin subordinate cocks, a process that ynymust thus consider the conditionsnecessary Guhl, Collias, and Allee (1945) term "psycho- for the evolution of deferred reproduction logical castration." This effect also occurs in among males. house mice (Lloyd, 1971). As older animals are The suggestionthat sexual bimaturismmight likelyto dominateyounger ones, the importance provide one key to the evolution of polygyny of social interactionsin the delayed reproduc- in grouse raises a number of questions, which tive maturationof males seems likely. the followingsections will consider. It is impor- In field experiments, the removal of older tant at the outset to separate clearlythe proxi- territorialmales oftenresults in disproportion- mateand ultimatecontrols of deferredbreeding ate recolonizationby younger males. Such re- by polygynous males (see Lack, 1954, 1965; sults have been obtained withBlue Grouse and Mayr, 1961; Orians, 1962). Accordingly,I will Ruffed Grouse, as reviewed above, and with considerthe development of male reproductive other birds (Orians, 1961; Krebs, 1971). behavior in polygynousspecies before consid- Apparentlythe presence of older males inhibits ering its evolution. the expression of territorial behavior by younger males. The behavioral mechanisms that this inhibitionremain largely un- Developmentof ReproductiveBehavior in Males produce explored. Young male Red-winged Blackbirds Delayed reproduction among males in po- only colonize vacancies late in the breeding lygynousspecies is associated with prolonged season (Orians, 1961). This observationsuggests physiologicalimmaturity. I have reviewedabove either that adult males become progressively the evidence for thiscorrelation among grouse, less motivated to establish new territories(see and similarpatterns of delayed maturationare Peek, 1971) or that first-yearmales become probably found in most polygynous birds. aggressive later in the season than do adults, Plumages of first-yearmales in polygynous or that both changes occur. species often resemble female plumages or are Other evidence suggests that social interac- intermediatebetween adult male and female tions with older males probably do not com- plumages (Crook, 1962, 1964; Selander, 1965). pletelydetermine the physiologicalimmaturity Among certain polygynous mammals young of young males. Field experimentsby Kirikov males usually reach full size only at about the (cited in Dementiev and Gladkov, 1967) indi- age when successful breeding begins (Carrick cated that young male Capercaillie retained the 216 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49 usual seasonal retardationin theiractivities even survival,delayed reproductionmust reduce an after all the older males had been removed individual's expected production of offspring. from their leks. Those first-yearmale Blue For delayed reproductionto evolve, this disad- Grouse thatobtain territorieshave testessimilar vantage must have compensations. Recent in size to those of other year-old males and mathematicalanalyses (Williams,1966a; Gadgil smallerthan those of older males (Bendell and and Bossert, 1970; Wiley, 1974) have suggested Elliott, 1967). In spite of this difference in that two conditions, when sufficientlypro- gonadal development, territorial first-year nounced, could favor the evolution of delayed males occupy areas of about the same size as reproduction: a high risk of mortalityduring those occupied by older males. However, they reproduction; and fecundity increasing with tend to abandon theirterritories earlier in the age. Lack (1954, 1968) had proposed these spring. It is not known whetherthose first-year explanations for the evolution of delayed males that establishterritories mate as success- breeding byboth sexes in a numberof monoga- fullyas older territorialmales. mous species. The developmental processes that regulate These arguments might also apply to de- the onset of successful breeding in males of ferred reproduction among males in polygy- polygynous species probably involve both (1) nous species, as Selander (1965, 1972) has behavioral interactions between older and recognized. If a young male, by reproducing, younger males, and (2) maturationalprocesses so jeopardizes his chances of survival to the independent of social interaction. To my followingbreeding season and yetgains a suffi- knowledge, no experiments on the control of cientlysmall expectationof progenythat would reproductivematuration in males have evaluat- survive to reproduce, then by breeding at an ed these two possibilities or have compared early age a male might actually reduce the related monogamous and polygynousspecies. disseminationof his genes in the population. As a result of any postponement of repro- Evolutionof DeferredReproduction among Males duction among males to a laterage than among females,the breeding sex ratio in a population The physiological and behavioral mecha- will increase. This ratio will also depend on nisms that control the development of repro- the age-specific survival rates of the sexes, as ductive capacity in males do not explain the sex ratios at hatching are about equal in birds selectionpressures behind theevolution of these regardlessof theirmating systems (Willson and ontogeneticprocesses. An explanation for the Pianka, 1963; Selander, 1960, 1965), and on evolution of any trait requires some demon- the rate of increase of the population. Could strationthat the traitincreases an individual's these increased chances formating at later ages fitness,the rate at whichan individualtransmits compensate for the effectsof postponed repro- his genes to his descendants. The rate at which duction on a male's rate of reproductive in- descendants propagate is specified by the rate crease? of reproductive increase, the Malthusian pa- To explore this possibilityI have calculated rameter (Lotka, 1956; Fisher, 1958). Unless the increase in fecunditythat would maintain some formof balancing selectionhas produced a rate of reproductiveincrease (r) equal to zero a stable polymorphism,genes associated with in spite of a delay in the onset of reproduction higher rates of propagation would eventually from Age 1 to Age a (Appendix; Fig. 2). This replace those associated with lower rates of value exactly equals the increase in expected propagation. Any lineage of a male and his fecundityof males that would result from de- sons that had a higher rate of reproductive layed reproductionby all males in a population increase would thus spread its genes in the from Age 1 to Age a (Appendix). Thus, an population relative to other genes. Females increase in the expected fecundity of males, would also acquire advantages in disseminating owing to sexual bimaturismin a stable popula- theirgenes by matingwith males withrelatively tion, would just compensate for the effectsof higher rates of reproductiveincrease. delayed reproductionon the rate of reproduc- The rate of reproductive increase depends tive increase for males. not only on fecunditybut also on the age of These calculations assumed a stable popula- reproduction. For any schedule of age-specific tion (r = 0). In reality, grouse populations SEPTEMBER 1974] EVOLUTION AMONG GROUSE 217

100 I 1.0

aa=l 2 -50- s 0.1 0.3 0.5 ab-aa +1 bb=ba

10 0.9 .1

0 1 5 10 0 .1 .5 1.0 a Sa

FIG. 2. THE INCREASE IN EXPECTED FECUNDITY, FIG. 3. PRE-BREEDING SURVIVAL WITH DELAYED b(a)/b(l), NEEDED TO MAINTAIN r = 0 WHEN THE AGE REPRODUCTION, Sb' AS A FUNCTION OF PRE-BREEDING AT ONSET OF REPRODUCTION Is DELAYED FROM AGE 1 SURVIVAL WITH EARLIER REPRODUCTION, Sa TO AGE a For both strategiesr = 0, althoughthe ages at The different curves represent different values of onsetof reproductiondiffer by one year (aa and pre-breeding survival, sl. See Appendix for derivation aa + 1) and theannual fecundity of a breedingmale of the functions. does not change. The differentcurves represent differentages, aa, at onsetof reproductionin the early-breedingstrategy. See Appendixfor derivation fluctuatein size considerably over periods of of thefunctions. several years,owing to changes in mortalityor fecundity,or both, from year to year. Lotka's standard equation for r, on the other hand, ed fecundity of a breeding male does not assumes that age-specificmortality and fecun- change, compensatoryincreases must occur in dity remain constant with time. In the long early survival. I have calculated, again when run, however, r usually averages close to 0, and r = 0, the increase in survival prior to repro- age-specific mortality and fecundity, when duction that will just compensate for a delay averaged over relativelylong periods, probably in the onset of reproduction from Age 1 to do remain nearlyconstant. In a steadilyincreas- Age a, when fecundity does not change ing population,the-proportion of youngerindi- (Appendix; Fig. 3). Thus, when delayed breed- viduals would be greater than in a steady ing is accompanied by this compensatory in- population, and consequentlythe expected fe- crease in early survival,a male's genes will just cundity of males in a population with sexual reproduce themselvesand thus will not change bimaturismwould also be greater. In this cir- in frequencyin a stable population. Any greater cumstance, therefore, males would have an increase in early survivalas a result of delayed expected rate of reproductiveincrease greater breeding, or any concurrent increase in later than 0, like the population as a whole. fecundity,would allow the relevant genes to A comparison of two populations, one with reproduce fasterthan the population as a whole. sexual bimaturism and one without, is not With sufficientlyreduced survival as a conse- strictlypertinent to the initial stages of the quence of early reproduction with or without evolution of bimaturism.Initially, in a popula- increasing fecundityat later ages, males that tion withoutsexual bimaturism,delayed repro- postpone the onset of breeding mightincrease duction by an individual male and his male the disseminationof their genes. descendants would not produce much change This conclusion takes into account the fact in their expected fecunditieslater in life. For that survivaland reproductionare not usually postponed breeding to evolve when the expect- independent attributesof an organism. The 218 THE QUARTERLYREVIEW OF BIOLOGY [VOLUME 49

limitedtime and energyavailable to an individ- survivalof the young, less experienced birds. ual are partitionedamong its various metabolic In view of the difficultiesin obtaining the activitiesor are temporarilystored in the form necessaryinformation regarding survival rates, of chemical bonds. Expenditure of time and a more practical approach might indirectly energy for reproduction is often incompatible measure the effectsof breeding on individual with expenditures for other activities,all of maintenance. Knowledge of the time- and en- which in differentways subserve the mainte- ergy-budgetsof breeding and non-breeding nance and growthof the organism. The alloca- males would indicate whether young, non- tion of time and energy at each stage of an breedingmales devote more timethan do adults individual's life to reproduction and mainte- to feeding,resting, and other activitiescontrib- nance will in part determine his age-specific utingto individualmaintenance. Positive results fecundityand survivaland the spread or persis- would suggest that breeding activitiesdo limit tence of his genes in the population. The genes the time available for individual maintenance. of individuals with more nearly optimal age- Comparisons made in both monogamous and specific allocations of time and energy should polygynousspecies of non-breedingand breed- prevail. At differentages there will pertain ing males would best elucidate the energetic differentoptimal compromisesbetween invest- basis forlife-history patterns in differentmating ing time and energy in reproduction and in- systems.These comparisonsare not yetavailable vestingtime and energy in individual mainte- for any species. Reports of lek-forminggrouse, nance. At older ages, as life-expectancyde- however, definitely imply that young males creases, natural selectionshould favora greater devote less time and energy to reproductive investmentof time and energyin reproduction. activities(see Wiley, 1973a). Although this approach provides a suitable Reproductive behavior and morphology frameworkfor analyzing the evolution of life- might also reduce survival by increasing the historypatterns (cf. Tinkle, Wilbur,and Tilley, conspicuousness or vulnerabilityof males to 1970; Tinkle and Ballinger, 1972), it has not predators. Among most of the promiscuous previously entered into discussions of the species of grouse, however,males acquire nearly evolution of mating systems.It seems probable full plumage in theirfirst year. Could year-old that the evolution of sexual differencesin life- males then have any advantage in avoiding historystrategies would contributeto the evolu- predators?Even full-plumagedmales are more tion of polygynous mating systems. Sexual or less camouflaged in theirenvironments until bimaturism, however, might not completely theyassume display postures. Only when neck explain thedistribution of matingsamong males ruffsare elevated, esophageal sacs inflated,and in polygynousspecies. Males of the same age tailsfanned do males become trulyconspicuous. could also differ systematicallyin mating Long-distancesounds also only accompany dis- success, a situationto be considered later (see plays. It appears plausible, then, that first-year below, Intrasexual Competition). males might reduce their encounters with predatorsby refrainingfrom display. Fights among males appear to have little Al- PossibleEffects of Reproductionon Survival in effecton survival in promiscuous grouse. Male Grouse though serious injuries are periodicallyreport- ed in the literature,in three seasons of work To demonstratethat deferred reproduction with Sage Grouse I never saw a male sustain enhances a young male's chances of survival an obvious injury in a fight. Hartzler (1972), would require a comparison of mortalityrates in his extensivework on thisspecies, also never among young males that engage in different observed a major injury. Fighting might still amounts of reproductive activity. That in- have indirecteffects on survival,as it represents formation would prove difficult to obtain. an appreciable expenditure of energy. Comparisons of mortalityin young, non-breed- Although the evidence is so far only circum- ing males and older, breeding males might stantial,it does seem plausible thatyoung male present difficultiesin interpretation,because grouse might actually enhance their survival reproductionmight have greatereffects on the appreciably by postponing reproduction. SEPTEIMBER 1974] EVOLUTION AMONG GROUSE 219

COMPETITION AMONG MALES AND THE EVOLUTION OF genes of the more fecund males will spread, FEMALE CHOICE provided again that the greater fecundityof these males does not entail overcompensating IntrasexualCompetition disadvantages in survival and later reproduction. Other conditions that might allow dif- One idea oftenadvanced since Darwin's time ferencesin fecundityto persistamong like-aged to explain-theevolution of postponed breeding males include formsof balancing selection,such in males of polygynousspecies is that year-old as heterosis, disruptive, or frequency-depen- males have less chance to mate successfullyin dent selection.Such variationwould also persist competition with older, more experienced if the differencesin fecundityarose at random males. This explanation defers the question, with respect to genetic differencesamong the since one must then explain why intrasexual males. competitiveabilities develop later rather than Individual differences in mating success earlier in life. If other featuresof theirlife his- among like-aged males of polygynous species, tories remained constant,males would do best although not fullydocumented for any species, to develop theirfull abilities for attracting mates are likelyto prove appreciable (forSage Grouse, early in life. For instance,if a certain intensity see Hartzler, 1972). Among males of a polygy- of displayor colorationwere necessaryto obtain nous species one might expect a pattern of mates, males that reached this level early in progressively increasing average fecundity life rather than later, without other changes throughout life, with considerable variance in life-historyparameters, would have the among individuals at each age. Far too little evolutionaryadvantage. Only when full repro- informationis available to compare the within- ductiveactivity at earlyages sufficientlyreduced age and the between-age variance in breeding early survivalwould deferred development of success among the males of any polygynous reproductiveabilities increase the rate of repro- species. At least in the lek-forminggrouse, both ductive increase for a male's genes. contributionsto the total variance in the dis- The evolutionaryconsequences of competi- tributionof matingsamong males are probably ton between males of differentages will thus substantial. depend on the consequences of competitionfor the males' life-historystrategies. Competition Female Choice with other males is one component of male reproductive activities. For the evolution of The behavioral and physiological mecha- delayed reproduction, the important thing is nismsthat regulate a female's choice of a mate thusnot competitionbetween males of different must once again not be confused with the ages but competitionbetween males with dif- selection pressures that explain why these be- ferentoverall life-historystrategies. havioralmechanisms increase a female's fitness. It bears repeating that developmental pro- The behavioral mechanisms that regulate a cesses do not explain evolution; instead, these female's choice might include differentialre- processesthemselves evolve to produce adapted sponses to variations in the behavior or mor- individuals. A demonstrationthat full repro- phology of individual males. In flocks of do- ductive capacity required two years of experi- mestic fowl, for instance, males that mate fre- ence would not mean that his developmental quently also frequentlyperform those displays process explained the evolution of delayed that lead to copulation (Lill, 1966). Ethologists reproduction.For an evolutionaryexplanation have also repeatedly demonstrated in experi- we need to know how a later development of mental situations that females in breeding intrasexualcompetitve abilities increases an in- condition prefer conspecific males with fully dividual male's fitness. developed secondary sexual characters, or Intrasexual competition between males of models that mimic these features(for instance, differentages needs to be distinguishedfrom Noble and Curtis, 1939; Hunsaker, 1962; Liley, intrasexual competition among males of the 1966). Such responses are clearly importantin same age. If inequities in the distributionof preventingdysgenic hybridization and in coor- matings pertain among like-aged males, the dinating reproductivebehavior in mated indi- 220 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49 viduals. It remains less clear, though, that they underlie a female's choice of a partner, these can completelyexplain the operation of polyg- mechanisms should evolve to maximize her ynous mating systemsin the field. chances of matingwith fit males and her breed- In my study of Sage Grouse, I concluded ing success. Unless delayed reproductionof the that the major behavioral differencesbetween male increased the spread of his genes, a fe- successful and unsuccessful adult males were male's genes would propagate faster if she the result,rather than the cause, of theirmore selected a youngermale and thus leftsons that persistent association with females (Wiley, would also tend to breed at an early age. In 1973a). Subsequently, Hartzler (1972) has general, then,females should not evolve mech- found some behavioral differencescorrelated anisms for choosing older mates, unless early with mating success that do seem to hold in breeding by a male decreases his fitness. comparisonsof adult males at similardistances An assertionthat femaleschoose older males fromfemales. Female Black Grouse apparently because these have demonstrated their ability respond differentlyto differencesin the tactics to survive (for instance, Robel, 1967; Koivisto, of displayingmales (Kruijt, de Vos, and Bosse- 1965) assumes incorrectly that male fitness ma, 1972; Kruijt and Hogan, 1967). These consistsonly in survival.Likewise, an assertion observers concluded that experience is neces- that a male's fitnessconsists in the number of sary before a male achieves full success in femaleswith which he matesis also only partially attractingfemales ready to copulate. Females correct,because reproductiverate depends not here base their choice on features of male onlyon fecunditybut also on theage of breeding behavior that develop withage. and on the consequences that breeding at a Although female choice mightrely partlyon given age have for survival. An explanation individual differences among males, female for the evolution of the females' behavior re- behavior could also include responses to other quires a full understanding of the adaptive females and to the environment.Female Sage significanceof males' life histories. Grouse arriving on a lek appear attracted to each other (Wiley, 1973a). One possibilityis thatfemales in this species remember the posi- EVOLUTION OF SEXUAL BIMATURISM: TENTATIVE tionsof matingcenters and tend to returnthere CONSIDERATIONS in subsequent years, and that older females attract younger ones to these sites. Evidence Granted thatthe adaptedness of sexual bima- for thispossibility is stillindirect; one difficulty turism might contribute to the evolution of is that the positionsof mating centerson some polygyny,what ecological differences might leks shift considerably from one year to the explain the evolution of sexual bimaturismin next,although thisseems not to occur on most some species of grouse but not others? Here leks. Female Long-billed Marsh Wrens appear again the correlationsbetween social structure to choose their nesting sites on the basis of and other attributescan provide some clues. the food supply or habitat within a male's The only identifiedcorrelates of sexual bima- territory rather than the male's behavior turism and polygynyamong the grouse are (Verner, 1963; Verner and Engelson, 1970). greater sexual dimorphism in size and larger This principle might apply to the females of overall size. The adaptive advantages of these other territorial,polygynous species as well characteristics,in the absence of overriding (Kluyver, 1955; Zimmerman, 1966; Wolf and disadvantages for single parental care, could Stiles, 1970). plausibly predispose a species to evolve sexual Female behavior thus might depend on at bimaturismand thus polygyny. least three sorts of stimuli: individual dif- Larger size mightprove adaptive for grouse ferences among males, behavior of other fe- because of changes in theirenergy balance and males, and characteristicsof particularsites or susceptibilityto predation. A larger size should featuresof the habitat.Certainly females might normally reduce the number of potential respond to more than one class of cues in predators and thus might increase life expec- choosing a mate. tancies. This possibility receives tentative Regardless of what behavioral mechanisms support from Helminen's (1963) studyof mor- SEPTEMBER 1974] EVOLUTION AMONG GROUSE 221 talityamong Black Grouse and Capercaillie in increase in proportion to the increase in her Finland (see above). Larger size, especially in existenceenergy requirements, egg production homeotherms, also entails proportionately could prove incompatible with larger size. In- lower rates of heat loss and consequentlyboth stead, to allow a large clutch, a female would lower metabolicrates per gram of body weight do betterto evolve a body size that maximized and greater resistance to temperaturefluctua- the margin between normal existence energy tions(Rensch, 1960; Kendeigh, 1972). For these requirementsand the rate of food acquisition. reasons, larger animals in a given biotope are That production of a clutch of eggs is in fact probablymore likelyto have population densi- a nutritionalstrain on a female is suggested ties consistentlynear the limitof resources. In by evidence that female grouse lay fewer eggs these circumstances, a greater emphasis on when food quality is low (Jenkins,Watson, and survival,especially early in life,might well favor Miller, 1967). In addition, unlike a male, a the spread of an individual'sgenes (MacArthur female grouse cannot increase her fecundity and Wilson, 1967; Pianka, 1972; MacArthur, by postponing breeding. Her annual fecundity 1972). Larger size mightin this way contribute will always equal the number of eggs she pro- to the evolution of deferred reproduction. For duces during her short breeding season. The grouse, the diversityof their mating systems potential advantages of postponing reproduc- and their life-historypatterns might thus tion at early ages in favor of greater survival depend in part on the diversityof their body are thus reduced for females. In polyandrous sizes. birds the selection pressures on female body Species differencesin body size among grouse size are probably very different (Jenni and are not easily explained with our present Collier, 1973). knowledge. The reason whysome species have Sexual dimorphism in size could also evolve not evolved large size might have to do with to reduce intersexual competition for limited the availabilityof their particularfood supply. food supplies (Selander, 1966, 1972; Schoener, It is particularlyat timesof food shortage that 1967, 1969). However, because the diets of all the additional food required by larger animals species of grouse are similarin kind,the advan- would put them at the greatest disadvantage. tages of reducing intraspecificcompetition for The energetic advantages of larger size pre- food thus seem equal for all. Nevertheless,this suppose that the amount of food an animal advantage mightcontribute to the evolution of can assimilate increases in proportion to the sexual dimorphismin size among grouse, even absolute increase in its energy requirements. if it does not completelyexplain it. Male and If this proportionalitydoes not obtain, animals female Capercaillie tend to feed in different might be expected to evolve a body size that parts of spruce trees, for instance (Seiskari, assured a minimum but sufficientmargin be- 1962). tween the amount of food an individual could A standard explanation for the evolution of collect per day and the amount normally re- sexual differencesin body size is thatlarge size quired for existence metabolism. The rate of is an advantage for males in intrasexual food acquisitionas a functionof body size would competition(Selander, 1972). A corollaryis that depend in turnon such factorsas the dispersion females are a more nearly optimal size for the and abundance of food items, the mobilityof species' particularfood habits and habitat. The the animal, and the animal's capacity to locate additional growth of males is thus viewed as and harvestthe food. one component of the male's reproductiveef- Sexual dimorphismin size and sexual bima- fort.In polygynousgrouse, however,first-year turismwould evolve if large size and delayed males attainvirtually full adult weight,although reproduction did not have the advantages for in other respectstheir reproductive physiology females thatthey do for males. Egg production remains immature. It would thus seem that requires an additional margin between the larger size is an advantage in itself to these amount of energy a female can collect as food younger males, independent of any advantage and the amount of energy she needs for exis- in reproduction. Among certain polygynous tencemetabolism. If the amount of food a larger mammals, on the other hand, males attain full female grouse could collect each day does not size only around the beginning of full repro- 222 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 49 ductive activity (Carrick et al., 1962; Geist, deferred reproduction probably increase in 1968a,b). Among thesemammals, then, changes saturatedenvironments. At least among grouse, in body size during a male's lifeparallel changes thiscondition should pertainespecially to those in other components of reproductiveeffort. with larger size. Deferred reproduction will Body size clearly evolves in response to a evolve more readily among male grouse than variety of selection pressures with complex among females,when a female's size is limited interactions. Energy balance, exposure to by the energyrequired for egg production,and predators, niche differentiation,and agonistic her annual fecundityis limitedto one clutch. success probably constitute only a partial list In other groups of birds as well, sexual of these selection pressures. Our present bimaturism and polygynyprobably correlate knowledge is insufficientto specifythe particu- with large overall size and sexual dimorphism lar ecological conditions that make larger size in size. Although thorough studies are needed and greatersexual dimorphismin size advanta- for verification,correlations between overall geous for some grouse and not others. The size and mating systemprobably obtain within adaptive pattern for polygynyamong grouse the Phasianidae, Cotingidae,Paradisaeidae, and neverthelessseems clear: for large grouse the Icteridae. In several tropical avian families, combination of larger males with postponed however,notably the Pipridae and Trochilidae, breeding and smaller females that lay large polygynyappears unrelated to size. At least in clutchesbeginning in theirfirst year evidently the Pipridae, polygynyis associated with sexual representsthe optimalcombination of male and bimaturism(D. W. Snow, 1962, 1963), as usual female life histories. The ecological circum- among birds and mammals. In these families stancesthat affect the evolutionof social systems the evolution of sexual bimaturismand polyg- among grouse thus probably act in part indi- ynypresumably depends on differentpatterns rectly,through their influence on the evolution of adaptation than those pertainingto grouse. of sexual differencesin body size and life-his- The general principlesunderlying the evolu- torystrategies. tion of polygynous mating systemsin grouse should, nevertheless,apply widely. Whenever sexual bimaturismis a concomitantof polygyny, CONCLUSIONS: A TWO-FACTORTHEORY FOR THE the evolution of mating systemsis inextricably EVOLUTION OF POLYGYNY associated with the evolution of sexual differencesin life-historystrategies. As a general Polygynyamong grouse has evolved as one rule, sexual bimaturismshould evolve when the component in a coadapted complex, which also optimal age-dependent expenditure of repro- includes adaptations in body size, life-history ductive effortdiffers for the two sexes. To the patterns,and parental care. Because polygyny extent that polygynyis incompatiblewith dual entails both sexual bimaturism and single parental care, the evolution of polygynywould parental care, polygyny should evolve only then depend on the relative advantages of when the advantages of deferred reproduction delayed reproductionin males and dual paren- among males outweigh any disadvantages of tal care. single parental care. When delayed reproduction occurs among males, single parental care and intrasexual competitionamong males are not alone sufficientconditions for the evolution ACKNOWLEDGMENTS of polygyny. The ecological conditions that influence the evolution of polygynousmating For stimulatingdicussions of manyideas in this systemsthus act through their dual effectsin paper,I especiallythank Peter Marler. In addition, received reducing the advantages of dual parental care helpfulsuggestions on themanuscript were from Gordon Orians, Jack Bradbury,Thomas the of and increasing advantages sexual bima- Schoener,Myron Baker, Helmut Mueller, and Alan turism. Feduccia.Linda Andersonand Ann Davis helped Among grouse, the evolutionof sexual bima- withtyping. This workwas supportedby an NIH turismappears related to the evolutionof sexual traininggrant to RockefellerUniversity (GM 01789), dimorphism in size and larger overall size of an NSF grantto P. Marler(GB 16606),and an NIMH the species. The evolutionary advantages of grant(MH 22316). SEPTEMBER 1974] EVOLUTION AMONG GROUSE 223

LIST OF LITERATURE

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VERNER,J., and M. F. WILLSON. 1966. The influence ZWICKEL, F. C., andJ. F. BENDELL. 1967. Early mortality of habitatson matingsystems of North American and the regulation of numbers in blue grouse. passerine birds. Ecology,47: 143-147. Can. J. Zool., 45: 817-851. , and __. 1969. Mating systems,sexual dimorphism, and the role of male North American APPENDIX passerine birds in the nesting cycle. Ornithol. Monogr.,9: 1-76. (1) The increase in fecunditythat is necessary to WATSON, A. 1965. A population study of ptarmigan compensate for a delay in the onset of reproduction (Lagopus mutus)in Scotland. J.Anim. Ecol., 34: from Age 1 to Age a, when r = 0: 135-172. Using the standard equation for discretebreeding . 1967. Population control by territorialbehav- seasons (Andrewarthaand Birch, 1954), iour in red grouse. Nature,215: 1274-1275. coD . 1972. The behaviour of the ptarmigan. Brit. 1 = , e--1 (x)m(x), Birds,65: 6-26, 93-117. x=O WATSON, A., and D. JENKINS. 1964. Notes on the behaviour of the red grouse. Brit. Birds, 57: and setting r = 0, m(x) = 0 when x < a, m(x) = = (a-,) S(,,-a) 137-170. b when x 2 a, and 1(x) s s where s is survival from Age 0 to Age 1, is annual survival , and __. 1968. Experiments on population sI control by territorialbehaviour in red grouse fromAge 1 to Age a, and s2 is annual survival after (Lagopus lagopus scoticus). J. Anim. Ecol., 37: Age a, we obtain 595-614. 1-b a:X 1 bs)S(a-1) WEEDEN, R. B. 1964. Spatial segregation of sexes in =Sj(la- 1) ES(X-I)= 1 rock and willow ptarmigan in winter. Auk, 81: x=l 1 S2 534-541. Consequently, . 1965a. Breeding density,reproductive success, and mortalityof rock ptarmiganat Eagle Creek, 1 -S2 b= --- centralAlaska, from 1960 to 1964. N. Am. Wildl. Conf.,30: 336-348. . 1965b. Grouseand Ptarmiganin Alaska. Alaska and Dept. Fish and Game, Juneau, Alaska. WILEY, R. H. 1973a. Territorialityand non-random b(a) - mating in sage grouse Centrocercusurophasianus. b(a= 1) Anim. Behav. Monogr.,6(2): 85-169. . 1973b. The strutdisplay of male sage grouse: (2) The increase in expected fecundityof males a "fixed" action pattern.Behaviour, 47: 129-152. that results from delayed reproduction of all males . 1974. Effectsof delayed reproductionon survi- in a population from Age 1 to Age a, when r = val, fecundity,and the rate of population in- 0: crease. Am. Natur.,in press. The expected fecundityof a male was taken as WILLIAMS, G. C. 196b6a.Natural selection, the costs the ratio of breeding females to breeding males, the of reproduction, and a refinement of Lack's reciprocal of the breeding sex ratio, which depends principle. Am. Natur., 100: 687-692. on the mortalityrates and ages at firstbreeding for . 1966b. Adaptationand Natural Selection.Prince- both sexes. I have assumed here that all males of ton UniversityPress, Princeton. breeding age fertilizeequal numbers of eggs each WILLIAMS,L. 1952. Breeding behavior of the Brewer year or, at least, that differencesin fecundityamong blackbird. Condor,54: 3-47. breeding males arise randomly. WILLSON, M. F. 1966. Breeding ecology of the yellow- If we assume a constant birthrate and a primary headed blackbird. Ecol. Monogr.,36: 51-77. sex ratio equal to one, then the reciprocal of the WILSON, M. F., and E. R. PIANKA. 1963. Sexual breeding sex ratio, selection, sex ratio, and mating system. Am. 00 Natur.,97: 405-407. E S,(1A-I)S(2x-1) WOLF, L. L., and F. G. STILES. 1970. Evolution of pair cooperation in a tropical hummingbird. 1/BSR= X=1 Evolution,24: 759-773. E s Xs(la 1) S(2X-1) WRIGHT, P. L., and M. H. WRIGHT. 1944. The reproductive cycle of the male red-winged blackbird. x=1 Condor,46: 46-59. where upper and lower case designate parameters ZIMMERMAN,J. L. 1966. Polygynyin the dickcissel. for females and males, respectively.If S, = Sj and Auk, 83: 534-546. A = 1, then SEPTEMBER 1974] EVOLUTION AMONG GROUSE 227

when r = 0 and fecundityof breeding males does not change: )S Here I compare two strategies,(a) one in which I1/BSR= -= the age at firstbreeding is a, s1 = s and s-= Csa' - a S(a1 ) (1 S2) c < 1; and (b) another in whichthe age at firstbreeding 1 S2 x=l is a + k, k an integer greater than 0, s = Sb, and s= The and and survival of Consequently, csb. fecundity(ba bb) breeding males (s2) is equal in both strategies. BSR (a) Using an equation derived in section (1) above, - S(la) BSR (a = 1) b = or sb = S(a/(a+k)) b S(a+k) a (3) The increase in early survivalthat will compen- a b sate for a delay of k years in the onset of breeding, Because a and k are both positive,sb > Sa.