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EXTRAPAIR FERTILIZATIONS AND THE EVOLUTION OF COLONIAL BREEDING IN PURPLE MARTINS

EUGENE S. MORTON, • LISA FORMAN, • AND MICHAEL BRAUN 2 •Departmentof ZoologicalResearch, National Zoological Park, Smithsonian Institution, Washington,D.C. 20008 USA, and 2Laboratoryof MolecularSystematics, Smithsonian Institution, Museum Support Center, Washington,D.C. 20560 USA

ABSTRACT.--Weused DNA fingerprinting to show that, in Purple Martins (Prognesubis), forcedextrapair copulations (FEPC) result in age-biasedextrapair fertilizations. Older males achieved96% paternity of their broodsand increasedtheir fecundityat the expenseof young males,which achievedonly 29%paternity. Older malesrecruit young malesand femalesto unusednesting cavities that they had previouslydefended against other older males.Each year, nearly half (45%)of the breedingmartins were recruitedyoung not born in the colony. Recruitmentsare individually timed and begin when each older male's mate has completeda nest. Adult malesmay have accruedan averageof 3.6 fertilized eggsthrough forced extrapaircopulations in addition to eggsproduced by their mates(4.5 eggs)for an overall average of 8.1. Noncolonial males without the opportunity for FEPCswould suffer 44%lower lifetime fecundity.Thirty-six percent of the eggsin the nestsof youngmales were the resultof egg parasitism,the significanceof which is unstudied.These findings support the hypothesisthat colonialbreeding evolved in Purple Martins to increasethe opportunity for extrapairfertilizations. Martins may be an extremeexample of a generaltrend in breeding systemswhere migrationand temperateclimate concentrate fertile femalesin time and space. Received26 May 1989, accepted12 October1989.

COLONIALbreeding has evolved often in birds The reason that Purple Martins nest coloni- that do not defend feeding territories, a trait ally in forested regions may be related to con- common in (Birkhead 1979, Gladstone straints not found in smaller of swal- 1979, McKinney et al. 1984, Wittenberger and lows or in other speciesof Prognethat breed in Hunt 1985, Emlen and Wrege 1986, Brown and the tropics.Monogamous pairing is standardin Brown1988a). Purple Martins ( subis) seem Purple Martins and the long breeding cycle (ca. to gain none of the many suggestedadvantages 64 days) restricts them to one nesting per year for colonial breeding in swallows (reviewed in (Allen and Nice 1952, Morton and Patterson Shields and Crook 1987). Colonial breeding in 1983). Martins are the world's largest swallows Purple Martins is not explained by predator sa- (ca. 56 g; i.e. ca. 12 g heavier than other Progne tiation (they do not nest synchronouslyand col- speciesand the African Mosque [Hi- ony size is small). They capture large, dispersed rundosenegalensis] Turner and Rose 1989). The food items to feed young (Walsh 1978),which young grow relatively slowly (Ricklefs 1968) precludesthe use of information from colony- and take 28 days to fledge after hatching. Both mates to locate prey concentrations,and they parents must feed for full-sized broods to sur- do not reducepredation by mobbing predators vive, and malesand females of older pairs share in large groups (Hoogland and Sherman 1976, equally in provisioning young (Allen and Nice Brown 1986, Brown and Brown 1987, Stutch- 1952, Morton 1987). Leffelaar and Robertson bury 1988). Martins take little individual risk (1986) discuss this requirement in the Tree in mobbing, fitting the pattern found in other Swallow (Tachycinetabicolor). Thus, fecundity colonial swallows (Brown and Hoogland 1986). cannot be increasedthrough multiple nesting Purple Martins would seem to gain no advan- or polygyny. tage, yet still have the costs, of group living. Males might overcomethis constraintthrough Costs include increased intraspecific competi- forced extrapair copulations (FEPC) (Brown tion for critical resources and increased ecto- 1978, Morton 1987), but no data are available parasite or diseasetransmission (Moss and Cam- on the successof FEPCsin achieving extrapair in 1970, Alexander 1974). fertilizations. In 1984, females that were not

275 The Auk 107:275-283. April 1990 276 MORTON,FORMAN, AND BRAUN [Auk,Vol. 107

Adult• F.E.P.C.'sSubadult• .100 ßTM After third yeai

o 'hird year

I-

Second year (estimated

ß 4 8 12 16 20 10 14 18 22 26 30 3 7 11

April May June DATE Fig. 1. (a) Percentageof final total breeding adults (after-third and third year) and subadult-plumaged (secondyear) PurpleMartins by date (solidlines: average for 3 yr, arrivalssummed over 3-dayintervals). Percentageof all nest-building females (either adult or subadult by date) is shown by dashed lines. The shadedarea showsdates of most intense forced extrapair copulationactivity (FEPCs)and is also the time of mostactive dawnsinging by adult males.(b) Number of eggs/day layed by matesof adult males(filled circles) and subadultmales (open squares)in 1987, in relation to the events in "a." guarded by their mates suffered an average of creasetheir fecunditythrough FEPCson newly 2.6 FEPCsper female in which cloacalcontact recruitedfemales, which pair with male SYs.If by the male with the female was observed. this is true, then male SYs should have lower Nevertheless,mate guarding was highly vari- paternity relative to male ASYs. We tested this able and its intensity was unrelated to the age hypothesis through the use of DNA finger- of the male (birds in their secondcalendar year printing. of life [SY]versus birds past the secondcalendar We show that FEPC successis achieved by year [ASY]). Individual males mate-guarded older males at the expenseof young ones,and from 0-100% during forays to the ground by it provides a sufficient source of selection to females to collect nest material, the main situ- favor colonial breeding and not favor nesting ation in which FEPCs are observed. Further- singly. more, no correlation was found between mate- guarding intensity by malesand their parental MATERIALS AND METHODS feeding effort (Morton 1987). Colonialbreeding behavior in martins.--Sixof the eight DNA fingerprinting (Jeffreyset al. 1985)pro- speciesin the New World Prognenest singly videsreliable informationon paternityand ma- (includes Phaeoprognetapera). However, the species ternity. Knowledge of the genetic parentageof limits in Progneare uncertain(AOU 1983).The Cuban young can enhanceunderstanding of behavior Martin (P. cryptoleuca)and (P. do- that otherwise appears enigmatic. Nocturnal, minicensis)may be colonialor noncolonial,depending predawn singing (dawnsong)by male ASYs upon nest-siteavailability (Wetmore and Swales1931). (Morton 1985) is one example. After-second- Gray-breasted Martins (P. chalybea)nest as isolated year malesbegin dawnsinging when their mates pairs and do not tolerateproximity even when pro- vided with a martin house(Beebe et al. 1917).Purple initiate egg laying (Morton pers. obs.).Because Martin males have a repertoire of song types acous- pairsare formed a month or more earlier, dawn- tically designedto overcomemasking in the "cocktail song does not function in this pair bonding. party" cacophonyof colonial breeding. Thesesongs, Second-yearbirds arrive at the colony in large used chiefly by males perched near defended nest numbers after dawnsinging begins (Fig. la). sites,have rhythmic syntax and end with a seriesof Morton (1988) hypothesizedthat male ASYsin- punctuatedpulsed notes.These differ from its dawn- April 1990] EvolutionofColonial Breeding 277 song (Morton 1985).Brown (1984) termed these"croak unbanded,by daily countsof individualsand by iden- songs"and Bitterbaum(1986) used "primary song," tificationof male SYs through their individualistic in a comparisonof Purple, Gray-breasted,and Carib- specklingof darkfeathers. The plumage of maleASYs beanmartins. songsare adaptedacous- is entirely purple,allowing easy distinction from that tically for use in colonial breeding, whereasother of SYs (Niles 1972a). The start of dawnsinging and Prognespecies use song for long-distancedefense of nestingchronology were recordeddaily. The colony isolatednesting sites. Volunteers, who wished to at- was housedin three 24-compartmentaluminum mar- tract martins to unoccupied martin houses,played tin houses(Trio Manufacturing Company) that can recordeddawnsong from early to mid-morning dur- be raised and lowered vertically on 4.3 m poles for ing SY arrival to attempt to attractSYs in the absence easy accessto the compartments. of live martins.A sampleof unoccupiedmartin houses We obtaineddata on mate guardingin 1984 and where playbackswere not performed were observed 1987 following methodsused earlier (Morton 1987). for comparison with those where they were per- If a female was followed by her mate when she left formed. their compartmentto collect nest material, this was Purple Martins breed colonially in forested areas tallied as one mate-guardedtrip. Nest material was of North America. Historically, they colonized dead gatheredwithin 40 m of the colonysite. We studied tree snagsthat had accumulatedwoodpecker holes 20 pairs daily from the initiation of nest building to (e.g. Wilson 1832). Most martins in western North nest completion(when the birds bring green leaves America use such sites (Allen and Nice 1952, Rich- plucked from trees to line the nest cup). mond 1953). There are few historicalreports of mar- DNA fingerprinting.--In1987, we obtainedblood tins breeding as isolated pairs in single-cavity sites samplesfrom 12 completefamilies (7 with male SYs in forestbiomes even though single-cavitysites are and 5 with male ASYs)of the 30 breedingpairs. Sam- more commonthan multiple-cavitysites (contra Brown pleswere obtainedfrom somebut not all mem- 1984). They rarely colonized cliff sites (Bent 1942). bers of the remaining 18 families. In these cases,the American Indians of the southeastern United States male or female roosted outside of the nest box on the grew a variety of the gourd (Lagenariasiceraria) spe- trappingnight. Two more familieswere completed cifically for Purple Martins (Speck 1941) and passed by the 1988capture of one female and one male that the longstandingtradition on to Europeancolonists. escapedcapture in 1987--for a final sampleof 7 SY Currently, in eastern North America, martins nest families and 7 ASY families. We had obtained mate- almostexclusively in gourdsor martin housespro- guardingdata previously(during nestbuilding) on vided by humans. These are best viewed as super- 13 of the 14 pairs. The number of feeding trips by normal stimuli for martins rather than as a cause of each pair member was recordedfrom two days of colonial nesting (see below). Purple Martins in the videotaped records (28 and 29 June 1987). Simulta- southwestern deserts of the United States, however, neousanalyses of feeding by all colonymembers con- nest solitarily in woodpeckerholes in saguarocacti trolled for weather effectson foraging conditions.To (Carnegieagigantea) (Phillips et al. 1964).Martins may controlfor differencesin age and number of young prefer the larger cavitiesmade by Northern Flickers between nests,we compared feeding rates of mates. (Colaptesauratus), which kill the cactus stem and, Bloodwas collectedby jugular venipuncture (0.25- therefore,do not accumulateto provide colony-nest- 1.0ml) in a heparinizedsyringe on 3 July1987. Whole ing potential(McAuliffe and Hendricks 1988).Here- blood was separatedby centrifugation,and packed after, we refer only to the colonial breeding popu- red cells were stored at -70øC. DNA extraction was lations of Purple Martins unless otherwise stated. accomplishedby standardprotocols that involve SDS/ Demographicprofile of thestudy colony.--We marked proteinaseK digestion, phenol/chloroform extrac- for individual identificationbreeding adults and their tion, and ethanol precipitation (Maniatus et al. 1982). young in a colony located in Severna Park, Anne We usedca. I0 #g of DNA in a 40 #1 reactionmixture Arundel County, Maryland. The nearestcolony is ca. to which 80 U of HinfI was added.The digestswere 5 km away.All young fledgedhad beenbanded since incubated overnight at 37øCand electrophoresedin the colony began (1976). Since 1979 (usually ca. 1 0.7% agaroseat 75 V for ca. 19 hours. Gels were de- July), adults were captured in their nesting cavities purinated in 0.25 M HC1, alkali denatured in 0.5 M at night by a speciallydesigned martin-house trap NaOH/1.5 M NaC1, and neutralized in 0.5 M Tris/3 (see Morton and Patterson 1983). A complete rela- M NaC1 before Southern transfer onto Amersham Hi- tionshipmatrix of the breedingadults was calculated bond membrane.The 33.6 minisatellitehybridization by J. Ballou (Ballou 1983). probe (Jeffreyset al. 1985) was radiaoctively labeled The colony is only 9 m from Morton's house,and by the primer extensionmethod with alpha 32P-dCTP the birds were observed and individuals identified to specificactivities of greaterthan 5 x 104cpm/#g. with a 40x telescopefrom a second-storywindow. Membraneswere hybridized overnight at 62øCin a The dates when banded ASY individuals arrived in buffer of 0.15 M NaC1, 0.015 M sodium citrate, 10% spring were recordedin 1986-1988.We estimatedthe dextransulphate, and 5 x 10? cpm/ml of probe. Wash numbers and arrival dates of SYs, most of which were stringenciesfollowed Jeffreys et al. (1985).Filters were 278 MORTON,FORMAN, AND BRAUN [Auk, Vol. 107

exposedfor 2-6 daysat -70øC with one intensifying martins (P = 0.02, Fisher exact probability test, screen.Final DNA fingerprintswere preparedby Siegel 1956). Additionally, male ASYs ceased Cellmark Diagnostics,Germantown, Maryland. All defending"extra" nesting compartments against comparisonsreported were from DNA fingerprints arriving male SYs(Rohwer and Niles 1979),al- on the sameautoradiograph. Autoradiographs were though they continuedto excludemale ASYs visuallyscored for bandsharing (following the meth- ods of Wetton et al. 1987 and Burke and Bruford 1987). and vigorously defended the cavity that con- tained their nest againstall males (pers.obs.). Finally, maleASYs began to attemptFEPCs with RESULTS nest-building females (Fig. la). DNA fingerprinting.--Wetested the effective- Chronologyand recruitment.--Coloniesform nessof FEPCin fertilizing extra eggsthrough when adults appear at their past breeding site DNA fingerprinting(Jeffreys et al. 1985,Wetton and then immigrantSY breedersarrive. After- et al. 1987, Burke and Bruford 1987). Purple second-year martins migrate to traditional Martin minisatellite phenotypes were ex- breedingsites a monthor morebefore SY breed- tremely variable. In one comparisonof eight ers (Allen and Nice 1952). At our site, adults unrelatedadults, we distinguisheda total of 65 arrived from 2 April until 11 May, and most bands,of which each averaged(+SE) 21.90 + were laying when SYsarrived (Fig. 1). Adults 0.398. Comparing these eight individuals in in their third year arrive later than older adults pairs,the probabilitythat a band presentin one but before mostSYs (Fig. la). is also present in another was 0.089. The prob- Adult malespair monogamouslyand nest in ability that all bands presentin one individual one cavity but defend extra nestholes in martin are presentin another is 0.0892•-9(< 10-24). houses from other adult males (Allen and Nice We made pairwise comparisonsof banding 1952). We found 2-6 extra compartments were patternswith the similaritycoefficient D, which usual, with a maximum of 24 (an entire house) varies from 0 (when no bands are shared) to 1 defended by one male. Brown (1979) reported (when all bands are identical) (Wetton et al. that up to 36 cavitieswere defendedby a single 1987).Parents and offspringwould be expected male. Subadultpairs began to occupythe extra to have D values ca. 0.500. We considered D nest cavities after ASY malesbegan to line their values <0.400 as genetic mismatchesbetween nestswith greenleaves (Morton 1987)and their putative parent and offspring.This is a conser- matesbegan to lay (Fig. lb). Most SYswere new vativevalue because the averageD (/•) value to the colony.Only 38 (25 malesand 13 females) for unrelated adults was 0.187 ñ 0.013 (n = 40 of 733 (5%) young fledged in 1976-1987 re- pairwise comparisonsbetween birds represent- turned to breed in their natal colony. From 1979 ed on the sameautoradiograph). After-second- to 1988, 236 of 527 (45%) breeding birds in the year and second-yearmales differed strikingly colony were new recruits.Most breedingASYs in paternity, regardlessof their mates'ages or are derived from birds first recruited as SY the intensity of mate guarding (Fig. 2). In male breeders (169 of 291, 58%). ASYs,b = 0.538+ 0.016,and only 1 of 28young The arrival of large numbersof SYscoincides was genetically mismatchedwith its putative with the beginning of dawnsinging by those father (Table 1). Second-yearmales fathered few male ASYs that are carrying green leavesto line of theyoung (7 of 24,29%) in theirnests (b = nests (Fig. la). Dawnsinging is an individual 0.288 + 0.032). In contrast, female SYs and ASYs performancefrom beginning to end and does did not differ as greatly in maternity,but 36% not involve any cooperation (e.g. flying as a of the young in femaleSY nests(n = 28) may group,synchronizing departure from the col- have resultedfrom egg parasitism(Table 1). In ony houses).Dawnsong lasts from ca.0415 until after-second-yearfemales, b = 0.536 + 0.025; 0540 EDT. Singingcommences in mid-May and in second-yearfemales, b = 0.420+ 0.019. ends in mid-Junein Maryland. A few male SYs The DNA fingerprints were also examined begin dawnsongsfor a few daysin mid- to late for band mismatches(Burke and Bruford 1987). June, after their matesbegin incubation. Play- Eachband in an offspringnot alsorepresented backs attracted one to three SYs at 3 of 5 pre- in one or both of the parentsis due to a mutation viously unusedmartin houses,whereas 0 of 10 or an extrapairfertilization. Single mismatched houseswhere dawnsongwas not played attract- bands were found in 2 of 28 young raised by ed martins. Playback significantly attracted male ASYs. An average of 4.95 + 0.481 mis- April I990] Evolutionof ColonialBreeding 279

100- ß t-I ß ß ß ß

90-

70-

60- E] SECOND YEAR

50- ß ADULT

30-

20-

10-

! ß I I I•1 I I I I I I 10 20 30 40 50 60 70 80 90 100

Percentage of trips mate-guarded Fig.2. Percentageof nestmaterial gathering trips that a maleguarded his mate against forced extrapair copulationsversus percentage of broodfathered as determined by DNA fingerprinting.

matchedbands per young was found in 19 of year males and their mates do not differ (78 vs. 24 young cared for by male SYs (Table 1). The 87 feedings per day, n = 11, T = 21.5, P > 0.05). mate of the only uncuckoldedmale SY in our sample(see Fig. 2) beganto lay on 14 June,after the time of abundantFEPCs (Fig. la). DISCUSSION The payoff to adult malesby nestingin sites with "extra" nesting cavities is enormous.If 3 Forcedextrapair fertilizations and the evolution of or more band mismatchesdefine a young ge- coloniality.--Althoughthe lack of territorial food netically unrelated to its male "parent," then defenseallows colonial breeding to evolve eas- 83%of the 1987young are unrelatedto the male ily in swallowsand other groups(Wittenberger SYsthat attendedthem. Because57 eggswere and Hunt 1985), colonial breeding in Purple laid in nestscontrolled by male SYs(Fig. lb), Martins is lesseasily explained. Members of one potentially 47.3 eggstotal--or 3.6 eggsper male Purple Martin population and of all the other ASY (n = 13 male ASYs in the colony)--were speciesof Progneare noncolonial breeders. Co- gained by FEPCs. If male ASYs did not have loniality in PurpleMartins is not simplyan an- the opportunityfor FEPCs,they would suffer cestralbreeding system. We believethat Purple 44% lower lifetime reproductive successthan Martins breedcolonially in forestedportions of thosein the studycolony. Obviously, this is an their rangebecause of a combinationof ecolog- averageand somemale ASYsundoubtedly are icaland genetic factors. Multicavitied tree snags more successful in FEPCs than others. are a necessaryecological background. The re- Second-yearmales adjustedto their low pa- strictedbreeding seasonof the TemperateZone ternity and fed young significantly less fre- climate and slow growth of young produce quently than their matesdid (51 vs. 67 feedings breeding constraints.Forced extrapair copula- per day, n = 10 pairs, T = 6.5, P < 0.05, Wilcoxin tion is the only way for males to increasefe- matched-pairssigned-rank test). After-second- cundity, and this may be enhancedby a cli- 280 MORTON,FORMAN, AND BRAUN [Auk,Vol. 107

TABLE1. D valuesfrom pairedcomparisons of PurpleMartin youngwith eachof their putativeparents, and the numberof bands(in parentheses)not foundin one or bothparents, calculated from DNA fingerprints usingJeffrey's Probe 33.6. Broods are separatedwith a spaceand arrangedaccording to the ageof the male parent.

Broods with male ASYs a Broods with male SYs a 0.519 (0) 0.436* 0.526(0) 0.632* 0.156 (3)0.563 0.418 (0) 0.540* 0.644 (0) 0.500 0.691 (0) 0.618 0.182 (4) 0.484 0.262 (3) 0.561 0.436 (0) 0.436 0.602 (0) 0.792 0.035 (5) 0.344 0.137 (5) 0.551 0.581 (0) 0.452 0.632 (0) 0.597 0.129 (9) 0.522 0.500 (0) 0.557 0.483 (0) 0.621 0.111 (4) 0.131 0.509 (0) 0.340 0.122 (3) 0.357 0.100 (4) 0.517 0.444(0) 0.545* 0.615(0) 0.582* 0.271(6) 0.456 0.367 (1) 0.720 0.577 (0) 0.509 0.308 (7) 0.500 0.400 (1) 0.714 0.509 (0) 0.448 0.308 (6) 0.411 0.333 (6) 0.340 0.464 (0) 0.702 0.423 (0) 0.436 0.286 (4) 0.515 0.146 (5) 0.250 0.576 (0) 0.435 0.244 (9) 0.250 0.472 (0) 0.409 0.586 (0) 0.531 0.542 (0) 0.375 0.679 (0) 0.475 0.444 (0) 0.525 0.523 (3) 0.576* 0.689 (0) 0.320 0.537 (0) 0.511 0.459 (0) 0.475 0.514 (1) 0.427 0.486 (0) 0.441 0.333 (7) 0.438 0.554 (0) 0.375 0.548 (0) 0.429 0.546 (0) 0.487 ßFemale ASYs are marked with an asterisk;for eachyoung, male D valueis on left, femaleD valueto the right of the numberof bandmismatches (in parentheses). matically restricted fertile period in females. own nests secure, attracted SYs to the colony The differencein breeding chronologybetween expressly to increase their fecundity. An at- SYs and ASYs is also important to enhance fe- tempting polygyny hypothesisseems unlikely cundity for ASYsthrough forcedextrapair cop- aspolygyny is virtually unknown in the species ulations. (Brown 1975) and has not occurredin our study Strong evidence in favor of this hypothesis colony in its 12-year history. An attempting comes from the enormous genetic payoff ac- polygyny hypothesisalso fails to explain male cruedby male ASYsthrough FEPCs.If extrapair SY recruitment.Early arrival of male and female fertilization successwas not relatedto age,then ASYs to colony sites might result from com- the proximate factors(discussed below) that un- petition for nest sitesin a secondarycavity-nest- derlie our hypothesis of colonial breeding in ing species(e.g. Stutchbury and Robertson1987). martins would remain only loosely related to Martins in the noncolonial southwestern pop- reproductive success.The genetic payoff is the ulations, however, return a month or more later ultimate reason in favor of colonial breeding. than more northerly colonial populations(Ca- The importance of breeding gregariously is ter 1944,Phillips et al. 1964). This suggeststhat highlighted by the fact that all FEPCsobserved nest-sitecompetition alone doesnot explain the were initiated by colonymembers (Morton 1987, early arrival of colonial populations. this study). There were no extracolonymales Delayed return of third-year birds (TYs), es- engaging in FEPCs.Furthermore, from the van- pecially males (Fig. la), may also be related to tage of its territory, a male is able to observe the competition for FEPCsthey encounter for favorite spots where females gather nest ma- the first time. Third-year birds are in adult terial. Males prone to attempt FEPCsoften wait plumage, and most have nestedbefore (as SYs) at these sites for the appearanceof unguarded in the colony. We note that male SYs have females(See Morton 1987 for a descriptionof undergone a complete, not a partial, molt (Roh- FEPC behavior). wer and Butcher 1988), by the time they breed The genetic data illustrate the importanceof (Niles 1972b, Klimkiewicz and Hill unpubl. many different factors that range from com- data). Thus the only difference between TYs munication to arrival chronology, to enhance and other age classesis that TYs are in adult the payoff for male ASYs. The timing of these plumage for the first time. As SYs,they "gave events suggestedthat male ASYs, with their up" eggs in return for a chance to nest without April1990] EvolutionofColonial Breeding 28! adult competition for nest sites. Now in adult 1984). This supports the precoitional display plumage,TYs are in competitionwith older birds hypothesisbut does not exclude an antiecto- for both nest sites and extrapair fertilizations parasitefunction for green leaf use in nestsby and must competefor nest-sitedominance. Purple Martins (Wireberger 1984). This hypothesiscan be testedby comparing Responseof male SYs to lowered paternity.--Male nestsites used between the second-yearto third- SYs respond to lowered paternity levels by year nestingwith thosebetween the third and feedingnestlings at a lower ratethan their mates. fourth year of age. A sample of 18 male SYs Male SYswill attemptto colonizea new nesting from 1984 to 1988 that returned to breed as site away from maleASYs, but singlemale SYs ASYs supportsthe difference in site dominance are not successfulin attracting mates.New col- suggested.Of 18 males, 17 changed nest boxes onies begin with a minimum of two nesting or compartmentswithin the same nest box be- pairs becausefemales will not nest alone with tween their second-and third-yearnestings. The an isolated male (Morton, pers. obs. of the un- changebetween nest sitesin TYs and the same successfulattempts of 3 isolated male SYs to individuals as4-year-olds was significantly less: attractmates vs. the successful"founding" of 8 only 6 of 11 changed location (x2 = 4.4899, df new coloniesby 2 or 3 male SYs).Females con- = 1, P < 0.05). Most of these changes were to strain second-yearmale options by avoiding compartmentsadjacent to their third-year sites. noncolonial breeding, which eliminates this Nest sites held as a breeding male SY did not option for male SYs. The male SYs that join translate into dominance at that nest site upon establishedcolonies forfeit ca.70% paternity but return to the colony as a TY. We speculatethat gain a nest compartment(one previously de- the timing of arrival is a balance between in- fended by a male ASY) and the presenceof creasedvulnerability to starvationfrom early multiple nesting pairs that attract potential spring cold weather (Mayfield 1969) and the mates.At the Maryland colony,male SYsthat genetic payoff accruedby having a completed did not attracta female by ca. 10 June did not nest and extra nest sitesby the time SYsarrive nest. Although males do not gain site domi- and are available for recruitment. We believe nance until nesting for the secondtime as TYs, that TYs, which do not have site dominance, most SYs returned to our breeding colony for avoid assymetricalcontests for nesting com- their entire lives. The lossof paternity in breed- partmentsby delaying arrival at coloniesuntil ing the first year may be balancedby a higher after-third-yearbirds (ATYs) have settledtheir lifetime geneticpayoff through FEPCs. contests.The middle arrival time of TYs rep- Eggparasitism.--We were surprisedto find that resentsan adaptivebalance (feeding conditions 36% of the young cared for by female SYs re- are adequate to support the increasedaggres- suited from egg parasitism.This rate is similar sion necessaryto fit into establishedmale ATY to the 22-43% of parasitizednests found in Cliff territories) and is early enough to establisha Swallows (Hitundo pyrrhonota) (Brown and nest and to be ready for FEPCs on the later Brown 1989). Unlike Cliff Swallows, however, arriving SYs. martins have not been observedto remove eggs Mate guarding.--Mate guarding has little to (Brown and Brown 1988a,b). Egg parasitesare do with assuranceof paternity (Fig. 2). Mate likely to be other femaleSYs rather than female guarding and its variability in martins most ASYs, as ASYs are incubating clutches when likely permit the female to complete nest parasitismoccurs and are unlikely to be laying building (Gladstone 1979, Morton 1987). The eggssimultaneously (Fig. lb). Perhapsthe fe- earlier a male completesa nest to assureits mo- male SYsbecome egg parasitesin part from the nogamoustybased annual fecundity, the more lack of parental effort from SY mates.However, time it can devote to FEPCs. Purple Martins the dynamics of this aspectof martin nesting carry green leaves to line the completed nest. biology remain unknown. This behavioris performedmainly by the mate Cuckoldrypotential relative to latitude.--The and may function as a precoitional display to high rate of cuckotdrywe found in Purple Mar- induce frequent copulation with its mate dur- tins may not be associatedentirely with the ing the female's most fertile period (Morton colonialbreeding system. Recently, other stud- 1987). In the tropical Gray-breastedMartin, ies of migratory, Temperate Zone passetines malesneither guard matesnor use green leaves showedhigher than expectedrates of cuckotdry in the nest(Morton unpubl. data,but seeDyrcz in monogamousspecies that defend large, all- 282 MORTON,FORMAN, AND BRAUN [Auk,Vol. 107 purpose territories. For example, 30-40% of breeding biology of the Purple Martin (Progne Indigo Buntings (Passerinacyanea) (Westneat subis).Am. Midl. Nat. 47: 606-665. 1987) and 34-38% in migratory populations of AMERICAN ORNITHOLOGISTS' UNION. 1983. Checklist White-crownedSparrow ( Zonotrichialeucophrys) of North American birds, 6th ed. Washington, D.C., Am. Ornithol. Union. (Sherman and Morton 1988) were conceived via BALLOU,J. 1983. Calculatinginbreeding coefficients FEPCs.Indeed, Quay (1989) documented sperm from pedigrees.Pp. 509-520 in Geneticsand con- transfer to femalesduring migration in the Ten- servation (C. M. Schonewald-Cox, S. M. Cham- nessee Warbler (Vermivoraperegrina). In con- bers,B. MacBryde,and L. Thomas,Eds.). Menlo trast, in nonmigratory Dunnocks (Prunellamod- Park, Benjamin/CummingsPubl. ularis), extrapair fertilizations were rare in BEEBE,W., G.I. HARTLEY,& P. G. HOWLS.1917. Trop- monogamouspairs (Burke et al. 1989). In con- ical wild life in British Guiana, vol. 1. New York, trast, females should avoid FEPCs for several New York Zool. Soc. reasons(Burke et al. 1989, Westneat et al. 1990), BENT, A.C. 1942. Life histories of North American not the least of which is injury. Cryptogamy is flycatchers,larks, swallows, and their allies. U.S. Natl. Mus. Bull. 179. one predicted mechanism used by females to BIRKHEAI),T.R. 1979. Mate guardingin the magpie avoid FEPCs.One way to be relatively cryptoga- Pica pica.Anim. Behav. 27: 866-874. mous is for females to look like males, but this BrrrERBALrM,E.J. 1986. The comparitive behavior of mechanismwill be stable only if nest building three speciesof swallows (genus Progne).Ph.D. is not correlated closely with fertility. In the dissertation, Gainesville, Univ. . Gray-breastedMartin, for example,nest build- BROWN,C.R. 1975. Polygamy in the Purple Martin. ing is highly synchronousin the late dry season Auk 92: 602-604. in central Panama (Morton unpubl. data), but --. 1978. Sexualchase in the Purple Martin. Auk 95: 588-590. egglaying is delayedand highly asynchronous. 1979. Territoriality in the Purple Martin. Wetmore et al. (1984) report nesting almost Wilson Bull. 91: 583-591. throughoutthe year. Significantly,the sexesare 1984. Vocalizations of the Purple Martin. alike in plumageas opposedto the extremely Condor 86: 433-442. sexually dichromaticPurple Martin. Tropical- 1986. colonies as information vs. temperate-breedingspecies of orioles(Icte- centers. Science 234: 83-85. russpp.) provide another example. The Purple --, & M. B. BROWN.1987. Group-living in Cliff Martin breeding systemmay, therefore, be an Swallowsas an advantagein avoidingpredators. extreme caseof a common system in the Tem- Behav. Ecol. Sociobiol. 21: 97-107. perate Zone. The pursuit of FEPCsmay have --, & . 1988a. A new form of reproductive more influence on avian biology, and with dif- parasitismin Cliff Swallows. Nature 331: 66-68. --, & . 1988b. Genetic evidence of mul- fering latitudinal consequences,than is cur- tiple parentagein broodsof Cliff Swallows. Be- rently appreciated. hav. Ecol. Sociobiol. 23: 379-387. --, & --. 1989. Behavioural dynamics of ACKNOWLEDGMENTS intraspecific brood parasitismin colonial Cliff Swallows. Anim. Behav. 37: 777-796. We thank C. Barkan, S. Beissinger,N. Belfiori, J. --, & J. L. HOOGL•ND. 1986. Risk in mobbing Blew, C. and C. Blohowiak, P. Davidar, K. and E. for solitary and colonial swallows.Anim. Behav. Derrickson, D. Gill, J. Gradwohl, R. Greenberg, S. 34: 1319-1323. Haig, S. Hunter, C. Johnson,K. Klimkiewicz, S. Ma- BURKE,T., & M. W. BRUFORD.1987. DNA finger- bey, M. V. McDonald, L. Morton, D. Niven, D. Nor- printing in birds. Nature 327: 149-151. man, R. M. Patterson,E. Shy, C. Smith, N. Tsipoura, --, N. B. DAVIES,M. W. BRUFORD,8r B. J. HARCH- and K. Young for field assistance,and R. and D. Boor- WELL.1989. Parentalcare and mating behaviour stin, J. and W. Belton, E. L. and J. Morton, and V. of polyandrousDunnocks Prunellamodularls re- Schneebelyfor help with dawnsongplaybacks. Sup- lated to paternity by DNA fingerprinting. Nature ported by ScholarlyStudies Grant 1235S603from the 338: 249-251. Smithsonian Institution. CATER,g. B. 1944. Roostinghabits of martins at Tucson, Arizona. Condor 46: 15-18.

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