Evolution, 38(2), 1984, pp. 327-341

SEXUAL SELECTION ON BODY SIZE, TERRITORY AND PLUMAGE VARIABLES IN A POPULATION OF DARWIN'S FINCHES

TREVOR D, PRICE Division ofBiological Sciences, The University ofMichigan, Ann Arbor, Michigan 48109

Received November 5, 1982. Revised May 9, 1983

Sexual selection on a phenotypic trait netic quality, male parental care or for arises when that trait covaries with mat­ resources that males control. Male ge­ ing success among individuals ofthe same netic quality has been subject to the most sex, usually males. As such sexual selec­ theoretical work, mainly because it is dif­ tion is thought to occur most readily and ficult to understand how genetic variance strongly in polygamous species where in male fitness can be maintained. One variance in mating success is high, but it explanation (lA in Table 1) is that nat­ can occur also in monogamous species ural selection opposes the sexual selec­ where there is competition among males tion, resulting in weak overall stabilizing for early breeding females (Darwin, 1871 selection (Fisher, 1958). An alternative Ch. 8; O'Donald, 1980). As Darwin orig­ model assumes that females choose males inally recognized, sexual selection in mo­ using as cues characters whose expres­ nogamous systems will be intensified sion correlates positively with overall ge­ when the sex ratio is skewed in favor of netic quality (1B in Table 1). These char­ males. This paper reports on sexual se­ acters can be termed facultative handicaps lection on male body size, plumage and (Maynard Smith, 1976; Zahavi, 1977; territory size characteristics in a small Andersson, 1982). Facultative handicaps population ofDarwin's Medium Ground may be defined as characters whose de­ Finches (Geospiza fortis) on I. Daphne gree of expression a) is used as a cue in Major, Galapagos, Ecuador. The species mate choice, b) has an associated cost (to is monogamous, but during this study prevent cheating) and c) is not solely de­ (from 1979 to 1981) males have outnum­ termined by genotype. Variance in over­ bered females by a factor ofthree to two. all male genetic quality can be main­ tained ifdifferent genotypes are ofhighest Theoretical Background quality in different generations, although The main purpose of this paper is to the maintenance of female mate prefer­ understand how the observed sexual se­ ences for the associated character re­ lection, to be described below, arose and quires that particular genotypes are fa­ is maintained. To do this I first present vored in runs ofseveral generations (i.e., a relevant theoretical classification of positive autocorrelation, Hamilton, 1982; types of sexual selection (Table 1). The Hamilton and Zuk, 1982). ultimate selection target (Table 1) is the Despite the appreciation that in many character which give a selective advan­ polygamous species male genetic quality tage to discriminating females. If differ­ is the only factor which can be involved, ences beween males in this character are the majority ofdemonstrations ofsexual not readily visible females are expected selection, especially those dealing with to use other cues to assess differences continuously varying traits, have been on among potential mates. Thus characters phenotypic characters whose variance is actually observed to be under selection, largely environmental and often age-re­ the proximate selection target in Table 1, lated (Howard, 1981; Johnson, 1982; may differ from the ultimate selection McLain, 1982; papers in Blum and Blum, target. Female preferences can be under­ 1979; reviewed by Halliday, 1978). The stood in terms of selection for male ge- sexual selection in such cases commonly 327 328 TREVOR D. PRICE

TABLE I. A classification of types of sexual selection.

Ultimate selection target Proximate selection target I) Male genetic quality: A) offspring, once mature, will be favored as mates A heritable character B) offspring are expected to survive well and be favored as mates A non-heritable character (facultative handicap) 2) Male parental care A non-heritable character (facultative handicap) 3) Resources a male controls The resources

arises from interactions among males and in an Appendix, and referred to in the from female preferences for resources that main body of the text where relevant. dominant males control (3 in Table l). Sexual selection based on resources or METHODS expected male parental care (2 in Table The Darwin's finches on the 40 hectare 1) is easy to understand. There is still the island, Daphne Major, have been inten­ question, ofparticular importance in this sively studied over the years 1976-1981: study, of how genetic variance is main­ in 1976-1978 by P. T. Boag (Boag, 1981) tained in a trait which cannot be inter­ and subsequently by myself. A descrip­ preted as a facultative handicap, and tion of the island can be found in Grant which is found to be correlated with mat­ et al. (1975) and Boag (1981). The island ing success. As discussed above, natural has been arbitrarily divided into 20 sec­ selection must be opposing the sexual se­ tors (Boag, 1981). These sectors fall nat­ lection or the trait must correlate some­ urally into four groups based on habitat times positively and sometimes nega­ type and plant composition, particularly tively with mating success. the relative abundance ofPortulaca how­ ellii, Opuntia echios and Bursera mala­ Scope ofthe Study cophylla. Comparisons of birds in these The central part of this paper will be groups are used in some tests. the observed selection on body size. Body Finch Measurements.-Finches have size characters are highly heritable traits been captured in mist nets throughout in this population (Boag and Grant, 1978; the study and five morphological mea­ Boag, 1983). Therefore observed sexual surements (three beak measures, wing selection has clear evolutionary impli­ chord, and weight) have been taken as cations. In addition, sexual selection oc­ described in Grant et al. (1975). Length curred on plumage coloration and terri­ measures were taken in millimeters and tory size. After demonstrating this, I will weight in grams. For many of the anal­ interpret the sexual selection on each yses beak depth is used as a measure of variable in the theoretical framework of body size. This is justified because beak Table 1. All three variables are weakly depth is highly correlated with other correlated and the interpretations rest on measures ofbody size, yet shows positive a consideration of each character sepa­ allometry with these measures and, most rately and when combined together. importantly, has low measurement error There are just two species of finches (Boag, 1981, 1983). All captured finches breeding on I. Daphne, Geospiza fortis were released unharmedcarrying a unique and G. scandens, the Cactus Finch. The combination ofcolorbands. By 1979, ap­ present paper concerns G. fortis. Geospi­ proximately 90% of all adult finches on za scandens was studied in less detail; the island were color banded (N = 217); results from this species are summarized by 1981 approximately 95% were color SEXUAL SELECTION IN FINCHES 329

TABLE 2. Estimated population sizes in March 1981, based on mapping pairs and territorial males on the island. The population is subdivided by co­ hort. The 1978 and 1979 columns give total num­ bers of birds hatched in those years and the 1976 column gives birds hatched in or before that year. There were no survivors from 1977 or 1980.

Unknown 1976 1978 1979 age Total Males 69 75 6 0 150 Females 24 41 II 3 79 % males 74 65 35 0 66

banded (population sizes are given in Ta­ ble 2). FIG. I. Categorization of plumage types. Males progress from the female-like plumage (Brown) in Finch Breeding. - Geospiza fortis sequence from Black-I to Black-5. Black-S is re­ breeds in response to rainfall which falls ferred to in the text as full adult plumage. erratically between January and June (Grant and Boag, 1980). In 1977 there was a drought resulting in no successful breeding and heavy adult mortality acquired any black when three years old (Grant and Grant, 1980; Boag and Grant, while others have been in virtually full 1981). The population sizes in the period adult plumage within 15 months of 1979-1981 have subsequently been so hatching. Once acquired, black plumage small that virtually all nests producing is never lost either seasonally or across fledged young have been detected; e.g., years. In each year the amount of black only two out of 190 (1%) were missed in plumage in each singing male was re­ 1981. All males build nests whether mat­ corded on an integer scale of one to five ed or unmated. These nests were marked (Fig. 1). Territories were delineated by and the males' mates, if any, were re­ the area over which males sang and by corded. Active nests were checked at two border displays. Territory size was mea­ to eight day intervals and information on sured in 1981, using a series of markers clutch size and hatching and fledging suc­ placed at 20 m intervals over the whole cess was collected. Chicks were color island. The presence or absence of im­ banded when eight days old. For present portant food plants in each territory was purposes a chick was assumed to have recorded. successfully fledged ifit reached this age, provided there was no evidence of sub­ RESULTS sequent mortality in or around the empty There are two different levels at which nest after this date. Laying and hatching sexual selection can be studied. The first dates were either directly observed or ex­ is to obtain an indication ofthe potential trapolated from chick development. for sexual selection through behavioral Plumage and Territory Measure­ observations ofpair formation and com­ ments. - Variation in plumage arises be­ parisons of variance in mating or repro­ cause young males resemble females, as ductive success between sexes or among commonly occurs in many sexually di­ populations and species (Payne and chromatic species (Darwin, 1871 Ch. 16; Payne, 1977; Wade and Arnold, 1980; Rohwer et al., 1980). The rate of acqui­ Payne, in press). The second is the direct sition of black (adult) plumage varies observation and interpretation of sexual considerably among individuals (Fig. 1). selection on a phenotypic character when In this study some males had scarcely that character correlates with differential 330 TREVOR D. PRICE

TABLE 3. Statistics on the mean and variance in mating and fledging success among males in each of three years. N: the number of color banded territorial males. Nm: the number of these males mated for at least part ofthe season. Vs: the binomial variance in mating success for males. Is: the squared coefficient of variation in mating success among males. x: mean number of chicks fledged per male. 1m: squared coefficient of variation in the number of fledged chicks per male. If the equivalent measure among females. The quotients Is/Im and Im/Ifare elaborated on in the text.

Year N Nm Vs Is 1m IJ Is/1m 1m/If 1979 82 54 .21 .49 .93 2.11 .88 .23 2.4 1980 158 64 .24 1.48 .13 15.60 5.57 .09 2.8 1981 142 85 .24 .68 1.93 1.12 .14 .62 8.0

mating success. Both levels will be con­ confronted by such males females fly off, sidered here in turn. or if on their own territory peck at the displaying male while awaiting the return Pair Formation of their mate to copulate. In such situa­ Immediately after rainfall, usually in tions I have observed three attempted January or February, territories are ex­ copulations on the back or wing of the panded so that in the more densely set­ female. tled areas there are well defined bound­ Mate Switches. -Some females change aries. Males build nests. Although mates between breeding bouts. Between experienced pairs may remain associ­ 1980and 1981, ten (18%) did so although ated, it is only at this time that inexpe­ at least four ofthese attempted to breed rienced females first acquire mates. Un­ with their original male; in each case the mated females arriving on territory are original male lost all or part of his ter­ chased in long twisting flights over and ritory to an unmated neighbor and the off the territory (sexual chases, e.g., Rat­ female then bred with the neighbor. Three cliffe, 1981) and may return, eventually other cases involved movement of over to build with the male. Within a few days 200 m by the female and cannot be so of pairing off the male may be regularly explained. feeding the female and eggs are usually The observations indicate that terri­ laid between eight days and one month torial interactions between males can in­ later. Sexual chases also commonly occur fluence mating success, but point to a sig­ between members ofpairs that have been nificant role in mate choice for the long mated. females, who can and do visit several ter­ Copulations Outside the Pair Bond.­ ritorial males before pairing. Females generally solicit copulations only from their own mates. I have once ob­ Variance in Mating and served a female mating with a neighbor­ Fledging Success ing male. This occurred after her mate (a Differential mating success among newly mated male) failed to respond. males is an indication ofthe potential for Males do not often attempt to restrict the sexual selection and can be quantified us­ movements of their females, and even ing the techniques of Wade and Arnold during egg laying many females spend a (1980; see also Payne, in press). Mating substantial time offtheir territory (see be­ success for a male is here defined as the low). presence or absence ofa mate. As a con­ Males regularly display to females to sequence of the skewed sex ratio (Table whom they are not mated, both on and 2) many males remained unmated, and off territory, and mated males may even none were mated bigamously. establish temporary second territories Statistics on the mean and variance for while their females are incubating. When various measures ofreproductive success SEXUAL SELECTION IN FINCHES 331

TABLE 4. Sexual selection on beak and body size. * = p < .05, ** = p < .01, and *** = p < .001 by two tailed t tests conducted on log transformed data to eliminate scale effects. The variances did not significantly differ in any comparison (Levene tests). See text for further details of the column headings. All entries for character values are means.

1979 1980 1981 Not mated Mated Not mated Mated Not mated Mated Weight 18.11 18.67 18.29 18.00 17.58 18.08 Wing 68.8 69.3 68.8 68.9 68.1* 69.8* Beak length 11.19 11.41 11.08 11.23 10.78** 11.15** Beak depth 9.97* 10.38* 9.90 10.03 9.67*** 10.16*** Beak width 9.01* 9.29* 8.96 9.06 8.81** 9.15** Sample size 54 28 21 31 59 46 are given in Table 3. The binomial vari­ paring the morphological traits of newly ance in mating success (Vs) is close to mated and unmated males. To avoid am­ .25, the highest possible in a monoga­ biguities, a pair is considered to be newly mous mating system. Is, the squaredcoef­ mated at the time when the first eggs are ficient of variation in mating success, laid. In addition I have included two pairs gives an approximate measure ofthe to­ that were known to be together for two tal opportunity for selection on a phe­ years before their first clutch was laid. notypic trait (Wade and Arnold, 1980). The morphometries are presented in Ta­ The squared coefficient of variation in ble 4 for three time periods, henceforth fledging success, lm, gives a measure of named by year. The 1979 column com­ variation in overall reproductive success pares all unmated adult males with those for the males. Thus the quotient Is/Lm mated in January of that year. No two gives the proportion of the variance in members ofa pair breeding in 1976 were fledging success that is directly attribut­ known to survive a drought in 1977; able to variance in mating success (Wade therefore the 1979 column rerpesents new and Arnold, 1980). In a year of high matings in 1978, with a reassortment of fledging success (e.g., 1981, Table 3) this an estimated three or four mates in 1979. may be very high. The breeding data from 1979 are used Squared coefficients of variation in instead of1978 because there was a higher fledging success among females (If) are proportion ofcolor-banded birds in that also given. The quotient Im/Ifis always year and because the population was more greater than unity (Table 3), confirming thoroughly studied. The 1980 column that the greater variance in mating suc­ compares those males that had acquired cess for males is translated into greater mates between January 1979 and April variance in more direct measures of re­ 1980 (mostly in May 1979) with those productive fitness, and that the potential that remained unmated; however two­ for sexual selection is higher among males year-old males are excluded in this com­ than among females. parison because so few (12%) acquired Both the behavioral observations and mates. The 1981 column is a comparison the large number of males that remain of newly mated with unmated males. unmated suggest that female choice of Table 4 shows that strong directional males is likely to be exercised to a far sexual selection for large size occurred in greater extent than male choice of fe­ two out ofthe three years. All traits show males. the same trend, although statistical sig­ nifiance varies: this is partly a reflection Sexual Selection on Beak and of differing measurement error among Body Characters traits (Boag, 1983). In this section I demonstrate sexual se­ Size Correlated Dominance. -One lection on body and beak size by com- common explanation for sexual selection 332 TREVOR D. PRICE is that larger males are dominant over cactus, in which 99.8% of all nests have smaller males and control resources such been built, but once the Opuntia has as food and nest sites that females prefer stopped flowering in February, it is not (Selander, 1972; Searcy, 1979a, 1979b). an important food source for many fe­ Dominance is difficult to observe directly males, and pairing up occurred after this in nature. Accordingly I induced a total time in 1980 and 1981. In 1981 Opuntia of 232 interactions at an artificial food area in territories did not correlate with source (bread crumbs) and recorded dis­ laying date among newly formed pairs placements of one bird by another. The (N = 32, r = - .13, P> .5). Over halfthe median size of birds dominated by an island was not defended by territorial individual (in beak depth or in body males but birds regularly foraged there. weight) was as often larger as smallerthan Females commonly foraged off territory the individual dominating (N = 19: 8 throughout the breeding cycle. Prior to larger, 9 smaller, with two ties). Experi­ laying males do feed females on pre-rains ments are likely to be inconclusive be­ food such as Opuntia seeds found mainly cause of uncontrolled variables such as on territory, but these seeds have been the different motivational states of the abundant throughout the study (Milling­ birds. To the extent that these observa­ ton and Grant, 1983). tions are applicable to dominance at the Both sexes regularly foraged off terri­ time ofterritory establishment, they give tory when feeding nestlings or recently no support to the idea of size-correlated fledged young. In 1981, in 33 continual dominance. However studies on other watches for 30 min of males or females bird species have demonstrated size-cor­ that were feeding nestlings or fledged related dominance (Baker and Fox, 1978; young, an average of 13.5 min (45%) was Searcy, 1979b). Size related dominance spent off the pair's own territory. certainly operates interspecifically on Portulaca howellii is the single most Daphne with larger congeners rarely being important food source during the breed­ displaced by smaller ones, and may op­ ing season, providing pollen, seeds and erate intersexually, for there was far caterpillars (Boag, 1981), but it occurs in greater mortality of females than males large areas out ofterritories and is found over a drought in 1977 (Boag and Grant, in just 60% of all territories. Portulaca 1981). seeds or pollen were found in 72% ofall If females choose males on the basis nestling crops examined in 1981 (N = of their resource holdings it should be 109) and occurred as often in territories 2 possible to identify these resources. Ter­ with Portulaca as without (X 1 = .25, P = ritory quality has been shown to be a .8). In 1979 and 1981 there was no dif­ major determinant ofmate choice in sev­ ference in mating success between males eral polygamous species (e.g., Pleszcyn­ with and without Portulaca on their ter­ 2 ska, 1978; Searcy, 1979c; Wittenberger, ritories (1979: N = 82, X 1 = .85, P = .4; 2 1981). Nest predation risks, potential 1981: N= 114, X 1 = .02, P= .9). In shade for the open nest and food supply 1980 the presence ofPortulaca correlated have been considered potentially impor­ with the chances of obtaining a mate 2 tant variables. In the present study suc­ (N = 52, X 1 = 4.55, P = .03). Much of cessful nest predation has never been the 1980 pairing took place in May 1979, known to occur. Potential shade is dif­ i.e., late in the season when Portulaca ficult to measure, but is unlikely to be had flowered and seeded and females were important because all finch nests are commonly foraging in it. By contrast, the domed and built deep in Opuntia bushes. bulk of pairing in the 1979 and 1981 I consider the possible importance of comparisons occurred when females were food supply first in enabling females to foraging on pre-rains food and on food accumulate resources for laying eggs, and (notably shoots ofannual plants) that re­ second in the feeding of nestlings. Ter­ sponded rapidly to the first rains. Both ritories nearly always include Opuntia these food types are distributed more SEXUAL SELECTION IN FINCHES 333 evenly over the whole island, occurring The natural selection for large size has abundantly in and out of territories. been interpreted as due to the superior I conclude that I cannot identify re­ large seed handling ability of larger in­ sources that distinguish territories that dividuals. This may be important in itself females might prefer. This is in contrast because males feed large seeds to the fe­ to G. scandens where Opuntia in terri­ males in the pre-laying period, although tories appears to be an important re­ large seeds are not commonly fed to nest­ source (Millington and Grant, 1983; Ap­ lings (Boag, 1981). Alternatively the pendix). higher survival probability oflarger males Active Female Choice.-A second pos­ may be reflected in a higher quality per­ sibility for the sexual selection is that fe­ sisting throughout the breeding season. males actively, regularly, choose males Consideration of the role of selection on on the basis of morphology (i.e., lA in other male characters lends support to Table 1). In principle the possibility of the idea that male quality is involved in active female choice is directly testable the sexual selection for body size. because there should be a genetic corre­ lation between mate preference and the Territory Size preferred male character (Lande, 1981). Despite the absence of identifiable re­ In one test for such an association I found sources in territories which could pro­ no correlation between females' fathers vide a basis for mate choice, territory area and their mates for any morphological per se, measured in 1981 only, was found trait (for beak depth r = .082, N = 19). to be an important predictor of mating However the expected magnitude ofthis success (probit analysis [Hanushek and correlation depends on the extent ofher­ Jackson, 1977] using log area, N = 93, itable variance in mate choice and may Xl, = 14.26, P = .0002). This trend was be very small, and its measurement is observed within each of the four habitat likely to be obscured by proximate eco­ types on the island, and was significant logical factors. Negative evidence is not in three of these areas. compelling. A very high correlation for territory Male Quality.-Both mechanisms of area was found among male sibs. Sib-sib sexual selection discussed above arise correlations can be used as an estimate from size differences between males of half the heritability of a character, al­ which are assessed either intrasexually (by though this estimate will be inflated (Fal­ males) or intersexually at the time ofpair coner, 1981). The intraclass correlation formation. There is evidence for another coefficient in a one-way analysis of vari­ effect: those males with recent high sur­ ance offull sib families using those males vival probability were favored as mates. hatched in 1978, is r = .50 (F[11,2l] = The two years (1979 and 1981) in which 3.73, P < .01). Part of this correlation sexual selection was observed followed may arise because there is a correlation periods of heavy (85%) and moderate between body size and territory size (see (20%) adult mortality, respectively. Pe­ below, Table 6), and body size is heri­ riods of adult mortality have been ac­ table. The effects of body size were re­ companied by selection for large size moved by regressing territory size on beak (Boag and Grant, 1981). Thus females depth and repeating the analysis using the have exercised a preference for large males residuals from the regression. This gave at just those times when large size was r = .43 (F[11,20] = 2.95, P < .05). The correlated with survival in the pre-mat­ correlation remains. The correlation does ing period. In 1980 little sexual selection not arise out ofa tendency ofbrothers to in G. fortis was observed and there had settle in similar habitats. When the island been very little adult mortality (hence no is divided into four parts only four pairs detectable natural selection) in the two of brothers settled in the same area. years previously. The above results were not anticipated. 334 TREVOR D. PRICE

It is worth noting that territory area is TABLE 5. Standardized partial regression coeffi­ determined anew at the beginning ofeach cients ({3) ± standard error when relative mating breeding bout. Neighbors, but not time success is regressed on beak depth, territory size ofsettlement, are likely to strongly influ­ and plumage. The R2 value for the regression and ence this variable. sample size (with the number of males obtaining mates in parentheses) are given. The column head­ Selection on Male Plumage ed adult males is a comparison of those males, at least two years old, which acquired mates in 1981 All the males that fledged in or before with those which remained unmated. The column 1976 were in or close to full adult plum­ headed 1978 males is a similar comparison for those age by 1981. Since many of the males males hatched in 1978 which acquired mates in from the 1978 and 1979 cohorts still re­ 1980 or 1981 with those that did not. ** P < .0 I. tained some sub-adult plumage, adult plumage is on the average an indicator Adult males 1978 males ofage. The differential rate ofacquisition {3 ± SE {3 ± SE ofblack plumage among members ofthe Beak depth .26 ± .10** .40 ± .14** 1978 and 1979 cohorts (relative numbers Territory area .30 ± .10** .24 ± .14 Plumage .24 ± .10** .26 ± .14 in Table 2) resulted in a large variance R2 .26** .26** to this character among birds breeding in Sample size 92 (43) 57 (24) 1980 or 1981. In 1981 females preferred males from these cohorts with more black in their plumage. Although plumage was recorded on a 1-5 scale (Fig. 1)there were scaled such that mean relative mating very few birds in the lowest plumage success equalled one. Log beak depth, log classes in 1981, and for comparisons in territory area and plumage recorded as that year I used presence or absence of presence or absence offull adult plumage full adult plumage (Black-5 in Fig. 1) as were separately standardized to have zero the variable in all statistical tests. Fifty mean and unit variance. In a preliminary five percent (N = 55) of the fully black stepwise multiple regression analysis males in the 1978 and 1979 cohorts ob­ other measures ofbody size and territory tained mates, whereas 29% (N = 63) of quality only entered after these measures, the males in some sub-adult plumage did and then did not contribute significantly. so. The difference is significant (x 2 = 8.15, All significance levels were checked using P = .004). With these data only a crude probit analysis (Hanushek and Jackson, estimate of the sib-sib correlation for 1977). 1978 hatched males in 1981 can be ob­ All three variables are individually un­ tained. In a one-way ANOVA the intra­ der highly significant directional selec­ class correlation coefficient was r = .24, tion of similar intensity (Table 5). Ifter­ F(ll,22) = 1.9, P = .1, although the as­ ritory size and plumage are added first to sumptions for statistical testing are vio­ the model, the significance ofbeak depth lated. is reduced from P = .001 to P = .01. This is because beak depth is correlated with Female Choice ofBody Size, Territory both territory area and plumage (Table Size and Plumage Combined 6). The separate results on body size, ter­ A second analysis was performed to ritory size and plumage for 1981 are sum­ determine the effects of the selection on marized in Figure 2. In this section I re­ just the 1978 cohort ofmales. Males from gress the dichotomous variable, male this cohort that acquired mates in either mating success, on these three characters 1980 or 1981 were compared with those to determine the relative strengths of se­ that did not (Table 5). Males from this lection acting directly on each character, cohort had significantly smaller territo­ following the methods of Lande and Ar­ ries than older males (N = 123, t = 3.3 nold (1983; Table 5). Mating success was P = .001) although they were not signif- SEXUAL SELECTION IN FINCHES 335

A TABLE 6. Pearson product moment correlations between log territory area and beak depth, and Spearman rank correlations between these char­ 2000 acters and plumage. The samples are as in Table 5, with adult males below the diagonal and 1978 males .. . above the diagonal. * P < .05. 1000 ~ .. .. Territory .. Beak depth area Plumage Beak depth .14 .16 400 .. Territory area .23* .14 '. Plumage .28* .23*

200

choice based on parental care that males 100c--1__---'-- -'--__---'-__--' 8.0 ~o 10~ 11~ 12.0 will provide. The character most ob­ BEAK DEPTH (mm.) viously indicating male quality is plum­ B age: experienced males are likely to be the best parents and might be identified by their adult plumage. 2000 However, a general difficulty arises with

E any tests because most males with non­

~ 1000 preferred characters remained unmated, w 0: hence their contribution to parental care « >­ cannot be assessed. It is also empirically 0: o difficult to assess contributions to paren­ ~ 400 .. , 0: tal care by those males that do breed. The W f- rate offeeding nestlings and females prior 200 to laying and during incubation can be observed but the amount of food per

100c--__---'--_--=--_'----__---'--__-" feeding, which varies substantially 8.0 9.0 10.0 11.0 12.0 (Downhower, 1978), cannot. In fact there BEAK DEPTH Imrn.) are small positive non-significant corre­ FIG. 2. The contributions of beak depth and lations of fledging success with territory 2 territory area to mating success. Symbols: • mated size (pro bit analysis, N = 44, x , = .8, males, ... unmated males. A) Males in full adult P = .7), and with the proportion ofadult plumage. B) Males retaining some juvenile plum­ age. plumage in males (Spearman's rank cor­ relation = .14, P > .5). Similar results are obtained when total nestling mass at age eight days or laying date are substi­ icantly smaller in beak depth (N = 130, tuted for fledging success. Trends, ifthey t = 1.6, P > .05). Beak depth is the only exist, are likely to be obscured by a large character under significant selection. random element to fledging success, There is no significant selection acting compounded by female contributions to directly on plumage or territory size (P > fledging success. One trend that can be .1 in each case). Associations of beak examined independently offemales is the depth with territory area and plumage are proportion of the brood fed by the male not significant (Table 6). once they have fledged. This is probably important because in this study females Male Quality only renested ifthey were feeding one or The question remains as to what ben­ no chicks. Again there is a trend towards efits females gain by choosing particular the blacker males taking a greater part in males. Here I consider the possibility of parental care, but it is not possible to test 336 TREVOR D. PRICE for significance. Figure 3 shows these data for males in 1981. 5 11-11-

DISCUSSION @4 ••11-0 1/-0 0 The Potential for Sexual Selection (9 0 W In the G.fortis population studied here ..J LL 3 11-11-11-0 there was high potential for sexual selec­ IT: • tion as measured by variance in mating mW :;;: and fledging success. These measures ap­ ~ •• 0 .0 proach those observed in some polyga­ 2 mous systems (cf. Payne, in press). Using the methods ofWade and Arnold (1980) 0 it was shown that about 50% of all vari­ ance in fledging success was attributable to having a mate. o I 2 3 4 Even though a high observed potential NUMBER FED BY MALE for sexual selection may often be ob­ FIG. 3. Number of fledglings in a brood com­ served, it is not always meaningful. Very pared with the total number of chicks fledged. "" a high coefficients of variation in mating male with some juvenile plumage, "* a male in full and fledging success in 1980 were of no adult plumage. The circled points are those where selective importance because all offspring the female laid a second clutch: note thai only fe­ males mated to males in full adult plumage had a died within one month offledging in that second clutch. year. Further, differences between years and between G. fortis and G. scandens in the potential for sexual selection (Appen­ dix) do not correlate well with the inten­ Table 1), correlating with aspects ofmale sities of selection acting on body size. quality, rather than directly genetically Measures of the potential for sexual se­ determined. Although heritability esti­ lection can only provide a crude approx­ mates using full sibs are inflated by the imation to its evolutionary importance. presence ofdominance and common en­ A similar conclusion has been reached vironment effects (Falconer, 1981) the from a large number of inter-species high estimates imply the presence ofsome comparisons (Payne, in press). additive genetic variance. However, as argued below, although the male quality Selection on Territory Size may be genetically based, the sexual se­ lection itself may be based on potential I now consider the observed selection parental care rather than on genetic con­ on each of the three phenotypic traits. I tributions to offspring. begin with the observed selection on ter­ Whatever the underlying cause, terri­ ritory size because the results are clearly tory size is a trait under sexual selection interpretable in terms of the theory (Ta­ in this population. Territory size per se ble 1). The main results for this character has been shown to be an important com­ are (1) territory size per se is important ponent ofmating success in Arctic Skuas, in mate choice and (2) sib-sib correla­ Stercorarius parasiticus (Davis and tions for territory size are high. O'Donald, 1976), and in several polyga­ The large difference in territory size in mous species territory size is correlated 1981 between males from the pre-1976 with the number of females a male se­ and from the 1978 cohorts, as well as an cures as mates (Armstrong, 1955; Balfour obvious immediate cost in maintaining and Cadbury, 1980). Sexual selection is a large territory, suggest that territory size a simple and general explanation for is a facultative handicap (1B and 2 in breeding season 'superterritoriality' dis- SEXUAL SELECTION IN FINCHES 337 cussed by Verner (1977). Similar ideas at the time of pair formation, less costly have been advanced by O'Donald (1977). when feeding their mates and hardly at all when feeding young. They thus appear Selection on Plumage Variation particularly suitable as indicators of po­ Several recent studies have demon­ tential parental care. strated that males with a greater propor­ tion ofthe adult coloration in their plum­ Selection on Body Size age are favored as mates (Proctor-Gray The selection on body size is the most and Holmes, 1981; Edwards, 1982; difficult to classify into clearly defined Payne, 1982). In this study males known alternatives. I consider each of the pos­ to be from the same age cohort were con­ sibilities outlined in Table 1 in tum. Both sistently at a mating disadvantage when schemes 1A and 1B in Table 1 are based in sub-adult plumage, and the same re­ on the idea that large body size is chosen sult was found for G. scandens (Appen­ because it is heritable, and there is an dix). Since sub-adult and adult territories advantage to having large offspring. In are interdispersed, this is not expected contrast under schemes (2) and (3) the from the hypothesis that presence of fe­ sexual selection arises because it corre­ male-like plumage is an adaptation that lates with future male parental care or enables young males to improve their resources males control. chances of obtaining a mate (Rohwer et (lA) Preferences for males are main­ al., 1980). tained by the mating advantage of their The alternative to an adaptive hypoth­ sons. The preferences could have arisen esis is that the acquisition ofadult plum­ out of a selective advantage in avoiding age is an indication ofmale quality. This heterospecific matings, for female Geo­ implies there is a cost associated with spiza are known to use beak and body adult plumage acquisition. One possibil­ morphology to distinguish among con­ ity is that plumage variation reflects un­ geners (Lack, 1947; Ratcliffe and Grant, derlying hormonal variation with asso­ 1983). One implication ofthis hypothesis ciated behavioral costs (Davis and is that large males are at a net disadvan­ O'Donald, 1976; Rohwer and Rohwer, tage under natural selection over a whole 1978). Males may also react more ag­ life cycle. The optimum body size under gressively to other males in full adult natural selection averaged over several plumage, simply because these males generations is unknown. represent a greater threat to their chances (l B) Body size could be under both of obtaining a mate. directional sexual and natural selection Sexual selection on plumage variabil­ over a whole life cycle in males. Once ity is more likely to arise out ofits general adult, males have been shown to be under indication of male age than its pheno­ natural selection for large body size (Boag typic handicap value. Older males could and Grant, 1981). The hypothesis is that be chosen either for their genetic quality females choosing males with high sur­ (as indicated by their continued survival) vival probability have sons which on av­ or estimated greater past breeding ex­ erage also survive well. This implies that perience. There are some indications that small body size will be naturally and sex­ males in full adult plumage contribute ually selected in other generations, and more parental care (Fig. 3), than those in females choose 'facultative handicaps' sub-adult plumage. (discussed below) that indicate male ge­ A possible genetic contribution re­ netic quality. This scheme appears un­ mains unassessed. However, corre­ likely because 1) there is no evidence for sponding to a decline in active territorial the required positive autocorrelation in defense, territory size and plumage are environmental conditions which favor both characters that are likely to be costly large size and 2) it is not clear that over 338 TREVOR D. PRICE a whole life cycle large males are at a with body size, and independently with survival advantage (Price and Grant, un­ previous male survival probability, then publ.). both types ofselection (2) and (3) on body There is a general argument against the size could arise from females preferring sole importance of schemes (1) in com­ those males with high survival probabil­ parison with (2) and (3) below. If male ity and using territory size as a cue. genetic quality were of major impor­ If natural selection is found to favor tance, females paired with inferior males small adult size just prior to breeding in might be expected to regularly 'steal cop­ a future year then the expected directions ulations' from higher quality males. This of sexual selection differ under the is not observed. schemes (2) and (3) and the relative im­ (2) Females choose on the basis ofmale portance of the two may be separated. quality because of the expected higher In summary, the interpretation of the contribution to parental care (including observed selection on all three characters feeding of the mate) high quality males which has the most support is that plum­ will make. One implication is that at age variation and territory size are facul­ present large size correlates with male tative handicaps chosen for their indi­ quality, which might be expected because cation of underlying male quality. Body large size correlated with survival prob­ size is partly selected because it correlates ability in the period immediately prior with quality at present. Quality is likely to breeding. Females choose males using to be realized in the contributions a male facultative handicaps. Territory size and makes to parental care and possibly to plumage have been identified from a some extent genetically to the offspring. multiple regression as two possible facul­ Other types of sexual selection on body tative handicaps correlated with body size are also likely to be involved. size, and some ofthe body size selection can be explained as resulting from selec­ SUMMARY tion for these two characters. In addition The population of Medium Ground unmeasured components (e.g., song rate, Finches (Geospiza fortis) on I. Daphne Greig-Smith [1982], and persistence in Major, Galapagos was studied between sexual chases) may also be involved. 1979 and 1981. During this period adult There is a substantial contribution of males outnumbered females by two or body size to mating success after the ef­ three to one as a result ofdifferential mor­ fects of territory size and plumage have tality during a drought in 1977. The been removed, especially within the 1978 skewed sex ratio resulted in a high po­ cohort of males. Therefore if scheme (2) tential for sexual selection in this mo­ is to account for much of the selection, nogamous species: about half the vari­ other cues ofquality correlated with body ance in male reproductive success was size must be important, or alternatively attributable to variation in mating suc­ females may use body size as a direct clue cess. Females preferred to mate with larg­ to quality in some years. er males in two out of three years. Ter­ (3) There is the possibility of sexual ritory size and extent of adult plumage selection on body size independent ofany were also found to be positively corre­ correlation with male quality. Under this lated with mating success, and all three hypothesis large males are dominant and characters contributed significantly when control resources that females prefer. Al­ combined into a regression model using though potentially important resources probit analysis. could not be identified, territory size is a The main conclusions for each of the variable directly involved in mate choice three characters treated separately are as that could be affected by size-related follows. Plumage and territory size char­ dominance. If territory size correlates acters are tentatively interpreted as being SEXUAL SELECTION IN FINCHES 339 indicators to females of male quality. BOAG, P. T., AND P. R. GRANT. 1978. Heritability High quality males probably contribute ofextemaI morphology in Darwin's finches. Na­ ture 273:793-794. increased parental care and possibly ge­ --. 1981. Intense natural selection in a pop­ netic quality to their offspring. I find no ulation ofDarwin's finches (Geospizinae) in the evidence that sub-adult plumage has Galapagos. Science 214:82-85. adaptive value with respect to mating DARWIN, CR. 1871. The Descent of Man and Selection in Relation to Sex. John Murray, Lon­ success. Territory size may be a sexually don. selected trait more commonly than is DAVIS, J. W. F., AND P. O'DONALD. 1976. Ter­ generally assumed and sexual selection ritory size, breeding time and mating preference may prove to be a general explanation in the Arctic Skua. Nature 260:774-775. for 'superterritoriality.' Body size was DOWNHOWER, J. F. 1978. Observations on the nesting of the Small Ground Finch Geospiza under selection in part because it posi­ fuliginosa and the Large Cactus Finch G. coni­ tively correlated with male quality; other rostris on Espanola, Galapagos. Ibis 120:340­ types of sexual selection (active female 346. preferences and male-male competition) EDWARDS, P. J. 1982. Plumage variation, terri­ toriality and breeding displays of the Golden may also be operating. Plover, Pluvialis apricaria in southwest Scot­ land. Ibis 124:88-95. ACKNOWLEDGMENTS FALCONER, D. S. 1981. Introduction to Quanti­ My thanks to Spike Millington and tative Genetics, 2nd ed. Longman, N.Y. Ayse Unal for companionship on FISHER, R. A. 1958. The Genetical Theory ofNat­ ural Selection, 2nd ed. Dover, N.Y. Daphne, and to Peter Grant for advice GRANT, P. R., AND P. T. BOAG. 1980. Rainfall on throughout, and drawing the birds. P. T. the Galapagos and the demography ofDarwin's Boag, J. F. Downhower, H. L. Gibbs, W. finches. Auk 97:227-244. D. Hamilton, R. Lande, S. Rohwer, D. GRANT, P. R., AND B. R. GRANT. 1980. Annual variation in finch numbers, foraging and food Schluter, P. E. Smouse and M. Zuk com­ supply on Isla Daphne Major, Galapagos. Oeco­ mented on the manuscript. This research logia 46:55-62. was funded by NSFgrants DEB-77-23377 GRANT, P. R., AND T. D. PRICE. 1981. Population and DEB-79-21119 to P. R. Grant, with variation in continuously varying traits as an some additional support from the Chap­ ecological genetics problem. Amer. Zool. 21:795­ 811. man Fund. GRANT, P. R., J. N. M. SMITH, B. R. GRANT, I. ABBOTT,ANDL.K.ABBOTT. 1975. Finchnum­ bers, owl predation and food supply on Isla LITERATURE CITED Daphne Major, Galapagos. Oecologia 19:239­ ANDERSSON, M. 1982. Sexual selection, natural 257. selection and quality advertisement. BioI.J. Linn. GREIG-SMITH, P. W. 1982. Song rates and parental Soc. 17:375-393. care by individual male Stonechats (Saxicola ARMSTRONG, E. A. 1955. The Wren. Collins, Lon­ torquata). Anim. Behav. 30:245-252. don. HALLIDAY, T. R. 1978. Sexual selection and mate BAKER, M. C, AND S. F. Fox. 1978. Dominance, choice, p. 180-203. In J. R. Krebs and N. B. survival, and enzyme polymorphism in Dark­ Davies (eds.), Behavioural Ecology: an Evolu­ eyed Juncos, Junco hyemalis. Evolution 32:697­ tionary Approach. Sinauer, Sunderland. 711. HAMILTON, W. D. 1982. Pathogens as causes of BALFOUR, E., AND C. J. CADBURY. 1980. Polyg­ genetic diversity in their host populations, p. yny, spacing and sex ratio among Hen Harriers 269-290. In R. M. Anderson and R. M. May Circus cyaneus in Orkney, Scotland. Omis. (eds.), Population Biology ofInfectious Disease Scand.10:133-141. Agents. Dahlem Konferenze, 1982. Verlag BLUM, M. S., AND N. A. BLUM, eds. 1979. Sexual Chemie, Weinheim. Selection and Reproductive Competition in In­ HAMILTON, W. D., AND M. ZUK. 1982. Heritable sects. Academic Press, N.Y. true fitness and bright plumage in birds: a role BOAG, P. T. 1981. Morphological variation in the for parasites? Science 218:384-387. Darwin's Finches (Geospizinae) ofDaphne Ma­ HANUSHEK, E. A., AND J. E. JACKSON. 1977. Sta­ jorIsland, Galapagos. Ph.D. thesis. McGill Univ. tistical Methods for the Social Sciences. Aca­ --. 1983. The heritability of external mor­ demic Press, N.Y. phology in Darwin's finches (Geospiza) on Isla HOWARD, R. D. 1981. Male age size distribution Daphne Major, Galapagos. Evolution 37:877­ and male mating success in bullfrogs, p. 61-77. 894. In R. D. Alexander and D. W. Tinkle (eds.), 340 TREVOR D. PRICE

Natural Selection and Social Behavior. Chiron signalling in Harris Sparrows: experimental Press, N.Y. deception achieved. Anim. Behav. 26: 1012­ JOHNSON, L. K. 1982. Sexual selection in a brentid 1022. weevil. Evolution 36:251-262. SEARCY, W. A. 1979a. Male characteristics and LACK, D. 1947. Darwin's Finches. Univ. Press pairing success in Red-winged Blackbirds. Auk Cambridge, Cambridge. 96:353-363. LANDE, R. 1981. Models of speciation by sexual ---. 1979b. Morphological correlates of re­ selection on polygenic traits. Proc. Nat. Acad. productive success in captive male Red-winged Sci. 78:3721-3725. Blackbirds. Condor 81:417-420. LANDE, R., AND S. J. ARNOLD. 1983. The mea­ ---. 1979c. Female choice ofmates: a general surement of selection on correlated characters. model for birds and its application to Red­ Evolution 37:1210-1226. winged Blackbirds (Agelaius phoeniceus). Amer. MAYNARD SMITH, J. 1976. Sexual selection and Natur. 114:77-100. the handicap principle. J. Theoret. BioI. 57:239­ SELANDER, R. K. 1972. Sexual selection and di­ 242. morphism in birds, p. 180-230. In 8. Campbell McLAIN, D. K. 1982. Behavioral and morpho­ (ed.), Sexual Selection and the Descent of Man logical correlates ofmale dominance and court­ 1871-1971. Aldine, Chicago. ship persistence in the blister beetle Epicauta VERNER, J. 1977. On the adaptive significance of pennsylvanica (Coleoptera:Meloidae). Amer. territoriality. Amer. Natur. 111:769-775. MidI. Nat. 107:396-403. WADE, M. J., AND S. J. ARNOLD. 1980. The in­ MILLINGTON, S. J., AND P. R. GRANT. 1983. Feed­ tensity of sexual selection in relation to male ing ecology and territoriality ofthe Cactus Finch sexual behaviour, female choice, and sperm pre­ Geospiza scandens on Isla Daphne Major, Ga­ cedence. Anim. Behav. 28:446-461. lapagos. Oecologia 58:76-83. WITTENBERGER, J. F. 1981. Male quality and O'DONALD, P. 1977. Sexual selection and the evo­ polygyny: the 'sexy son' hypothesis revisited. lution of territoriality in birds, p. 113-129. In Amer. Natur. 117:329-342. F. 8. Christiansen and T. M. Fenchel (eds.), ZAHA VI, A. 1977. The cost of honesty (further Measuring Selection in Natural Populations, remarks on the handicap principle). J. Theoret. Lecture Notesin Biomathematics.Springer-Ver­ BioI. 67:603-605. lag, N.Y. ---. 1980. Sexual selection by female choice Corresponding Editor: R. Ricklefs in a monogamous bird: Darwin's theory cor­ roborated. Heredity 33: 1-16. PAYNE, R. 8. 1982. Ecological consequences of song matching: breeding success and intraspe­ ApPENDIX cific mimicry in Indigo Buntings. Ecology 63: Sexual selection on Geospiza scandens. - As in 401-411. G.fortis the sex ratio in G. scandens has been skewed ---. In press. Sexual selection, lek and arena towards males since 1977 (Millington and Grant, behavior and sexual size dimorphism in birds. 1983). The potential for sexual selection was as Ornithol. Monogr. great as in G. fortis, as shown by a partitioning of PAYNE, R. 8., AND K. PAYNE. 1977. Socialorga­ the components of potential selection (Table AI). nization and mating success in local song pop­ G. scandens differs in being less variable in both ulations ofVillage Indigobirds, Vidua chalybea­ body size and in rate of plumage acquisition: only tao Z. Tierpsychol. 45: 113-173. two out of 39 males (5%) were not in full adult PLESZCYNSKA, W. K. 1978. Microgeographic pre­ plumage by their third year. There was no signifi­ diction ofpolygyny in the Lark Bunting. Science cant directional selection on male body size accom­ 201:935-937. panying the mortality of 1977 and no directional PROCTOR-GRAY, E., AND R. T. HOLMES. 1981. sexual selection in 1979 or 1980 (Table A2). How­ Adaptive significance of delayed attainment of ever it is notable that there was stabilizing selection plumage in male American Redstarts: tests of on beak length over the period of mortality (Grant two hypotheses. Evolution 35:742-751. and Price, 1981) and the variance decrease for this RATCLIFFE, L. M. 1981. Species recognition in character under sexual selection in 1979 was close Darwin's Ground Finches (Geospiza, Gould). to significance (P = .06, two-tailed Levene test). Di­ Ph.D. Dissertation. McGill Univ. rectional sexual selection was observed in 1981, but RATCLIFFE, L. M., AND P. R. GRANT. 1983. Species this was not preceded by substantial mortality. recognition in Darwin's Ground Finches (Geo­ Among the males hatched in 1978, those with spiza, Gould). I. Discrimination by morpho­ more fully adult plumage were favored as mates in logical cues. Anim. Behav. 31:1139-1153. 1980 (probit, N = 45, x2 = 6.8, P = .009). Geospiza ROHWER, S., S. D. FRETWELL, AND D. M. NILES. scandens differs from G. fortis in holding defined 1980. Delayed maturation in passerine plum­ territories throughout the year; female choice may ages and the deceptive acquisition ofresources. be based on cactus quality which is important for Amer. Natur. 115:400-437. survival and early breeding (Millington and Grant, ROHWER, S., AND F. C. ROHWER. 1978. Status 1983). In 1979, area ofcactus correlated with male SEXUAL SELECTION IN FINCHES 341 size but mating success did not. A more direct mea­ (Millington and Grant, 1983). Territory area and sure of territory quality (number of cactus fruits) other variables have not been measured in subse­ correlated with mating success but not male size quent years.

TABLE A 1. Statistics on mating and fledging success in Geospiza scandens. Conventions and comparisons as in Table 3.

Year Nm Vs 15 .\" 1m 1/ Is/1m Im/Lf 1979 62 25 .24 1.50 .89 2.80 .28 .54 10.0 1980 104 50 .25 1.09 .66 2.73 .80 .40 3.4 1981 98 58 .24 .70 1.62 1.13 .13 .62 8.7

TABLE A2. Size selection in Geospiza scandens. All conventions and comparisons are as used in Table 4. With the exception of wing length, which was significantly less variable among the mated males than the unmated males in 1980 (P < .05), there were no significant differences in the variance for any character (Levene tests).

1979 1980 1981 Not mated Mated Not mated Mated Not mated Mated Weight 21.41 * 22.71* 21.66 21.18 21.16 21.63 Wing 74.42 74.88 74.38 74.40 73.00 73.64 Beak length 14.69 14.85 14.89 14.54 14.39 14.64 Beak depth 9.47 9.59 9.56 9.41 9.33* 9.55* Beak width 8.90 8.88 8.89 8.89 8.69* 8.95* Sample size 41 16 16 25 35 25