Anatomical Adaptations to Sperm Competition in Smith's Longspurs and Other Polygynandrous Passerines
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The Auk 110(4):875-888, 1993 ANATOMICAL ADAPTATIONS TO SPERM COMPETITION IN SMITH'S LONGSPURS AND OTHER POLYGYNANDROUS PASSERINES JAMES V. BRISKIE Departmentof Biology,Queen's University, Kingston, Ontario K7L 3N6, Canada';and Departmentof Animaland Plant Sciences,University of Sheffield, P.O. Box601, Sheffield,S10 2UQ, UnitedKingdom AI•STRACT.--Icompared the reproductiveanatomy of the polygynandrousSmith's Longspur (Calcariuspictus) with two other polygynandrouspasserines (Dunnock [Prunellamodularis] and Alpine Accentor[P. collaris])and with a wide rangeof sociallymonogamous species. All three polygynandrousspecies were found to have enlarged testesand cloacalprotuberances (i.e. the site of sperm storage)compared to specieswith other mating systems.Testes lengths in polygynandrousspecies averaged 44% longer and cloacalprotuberances 213% greater in volume than expectedfor the body sizesof these species.Testes mass in Smith's Longspurs comprised4.2% of adult body massor more than twice (2.0%) that found in the congeneric and monogamousLapland Longspur(C. lapponicus).Smith's Longspurs also had larger cloacal protuberances,larger seminal glomeraand higher spermstores, suggesting a greateroverall rate of spermproduction than in LaplandLongspurs. In contrast,females of polygynandrous speciesdid not show any consistentdifferences in the pattern of sperm storage due to increasedsperm production by males,although this needsto be evaluatedmore thoroughly. The enlarged male reproductive organs of Smith's Longspursand other polygynandrous speciesappear to have evolvedas a consequenceof spermcompetition, whereby large sperm reservesfunction to insure paternity through diluting or displacingthe ejaculatesof rival males.Received 26 December1991, accepted 25 November1992. SPERM COMPETITION results whenever females specific comparisonsof primates (Harcourt et mate with more than one male during the span al. 1981,Harvey and Harcourt 1984),birds (Car- of a single breeding attempt (Parker 1970). Al- tar 1985,Moller 1991)and mammals(Kenagy thoughmultimale mating may be advantageous and Trombulak 1986, Brownell and Rails 1986) to females in somesituations (e.g. Smith 1988, have shown that nonmonogamousanimals have Moller 1988a),it can alsoreduce a partner'spa- relatively larger testesthan monogamousspe- ternity (e.g. Gibbset al. 1990). To counter female cies.Since larger testes produce more and larger infidelity and increasethe probabilityof pater- ejaculates(Moller 1988b), an increasein testes nity, males have evolved several elaborate size has been interpreted as an adaptation to counter measures.For example, males in some sperm competition (Harcourt et al. 1981, Moller speciescontinually guard and defend their mates 1988b, 1991). from the advancesof other malesduring the Smith's Longspurs (Calcariuspictus) are un- period when eggsare fertilizable (Beecherand usualamong passerine birds in that femalesreg- Beecher1979, Birkhead 1979). If extrapaircop- ularly pair and copulatewith more than one ulationsoccur, then pair malesmay reducetheir male for a singleclutch of eggsat the sametime subsequentparental investment to avoid wast- that males pair and copulate with several fe- ing energyor resourceson raisinganother male's males (Briskie 1992). In a color-bandedpopu- offspring (Trivers 1972, Burke et al. 1989). lation near Churchill, Manitoba, 76.2% of 21 Sometimesfemale infidelity cannot be pre- females observed mated with two males, 9.5% vented becauseof ecological constraints,but with three males,and only 14.3%with a single malesmay nonethelessincrease paternity con- male (Briskie 1992, 1993). Of 27 males observed fidencethrough frequent copulationsthat di- in the same population, 63.0% mated with two lute or displacerival ejaculates(McKinney et females, 7.4% with three females, and 29.6% with al. 1984, Birkhead et al. 1987). Indeed, inter- a singlefemale. This combinationof polyandry and polygynyis termedpolygynandry and has been reported in only two other passerinesto Present address. date (Dunnock, Prunellamodularis [Davies 1985] 875 876 JAM•SV. BRISKIE [Auk,Vol. 110 and Alpine Accentor, P. collaris [Nakamura 1954,Salt 1954).Sperm producedin the testesmature 1990]). Males in all three speciesassist females in the glomera and are stored there until ejaculated. in feeding offspring; in Smith's Longspurs as Both sperm production and sperm storage capacity many as three males may provide food at a sin- are expected to increase as an adaptation to sperm competition (e.g. Smith 1984); thus, males in species gle nest (Briskie 1993). Becausefemales copulate exposedto high levels of sperm competition should with severalmales during the period when eggs have suchorgans enlarged relative to thosefound in could be fertilized, males risk investing energy monogamous species. in offspring fathered by another male. Possibly Cloacal protuberanceswere measured on 29 pas- to minimize this cost,copulations in these spe- sefine species breeding in Ontario and Manitoba, cies are extraordinarily frequent and, in the Canada from 1988 to 1991 (see Table 1 for a list of Smith's Longspur, average more than 350 per species).Apart from the Smith's Longspur,this sam- clutch (Briskie 1992). Observations of such ex- ple included 2 socially polygynousspecies (Yellow- treme behavior, along with recent findings of headed Blackbird [Xanthocephalusxanthocephalus], high levels of mixed paternity in the Dunnock Brown-headed Cowbird [Molothrus ater]), 2 sequen- tially polyandrousspecies (American Goldfinch [Car- (Burke et al. 1989) and Smith's Longspur (75% duelistristis], Common Redpoll [C. fiammea])and 24 of 12 broods with mixed paternity; R. Mont- sociallymonogamous species (all remaining species goreerie, J. V. Briskie and T. Poldmaa unpubl. listed in Table 1; mating-systemdata from Ehrlich et data), strongly suggestthat intense sperm com- al. 1988, Briskie and Montgomerie 1992, and refer- petition is commonin all polygynandrousspe- encestherein). Using calipers,I measured(to 0.1 mm) cies. the diameter (along left-right axis) and height (on In an earlier paper, I described how sperm one side) of the cloacalprotuberance on each male competition has influenced the mating behav- captured or collected from one week before to one ior of Smith's Longspurs(Briskie 1992). Here, ! week after the peak clutch-initiation period of that examine the reproductiveanatomy of this spe- species. Clutch-initiation dates were determined by direct observationsand most males were captured or cies to determine what adaptations have arisen collected at known nest sites or on territories with to cope with the high levels of sperm compe- nesting females. Becausecloacal-protuberance size tition experienced by males. Recently, Naka- varies over the breeding cycle, for all interspecific mura (1990) and Birkhead et al. (1991) examined comparisonsI used only data from those birds mea- Alpine Accentorsand Dunnocks, respectively, sured during the peak period of clutch initiation; this for the purposeof determining how spermcom- is the period when cloacal protuberance size is at its petition has affected male and female repro- maximum (Quay 1986, Weatherhead and Robertson ductive anatomyin thesespecies. Males in both 1980, unpubl. data). Using these values, I estimated specieswere found to have very large testesand cloacal-protuberancevolume as h•rr•, where h is the cloacalprotuberances (i.e. the site of spermstor- cloacal-protuberanceheight and r is 0.5 timesthe pro- tuberance diameter. Sample sizes per speciesranged age) but in neither study was enough infor- from 1 to 37 (Table 1). mation available to make detailed comparisons To examine the structure of the seminal glomera with socially monogamousspecies. I collected and cloaca in greater detail, I collected five male data on cloacal-protuberancesize, testissize, and Smith's Longspurs:three during their copulationpe- sperm-storagepatterns for a wide variety of riod, one after the copulation period, and one post- North American passerines.Using the data from breeding bird. Within an hour of death, the cloacal Alpine Accentors and Dunnocks, ! then exam- protuberancewas removed and preservedin 10%buf- ine how sperm competition has influenced the fered formalin. Each seminal glomerus was later dis- reproductive anatomiesin all three polygynan- sected,measured and weighed. To estimatethe num- drous species. ber of sperm stored by each male, I finely minced each glomerus and washed the sperm into a known METHODS volume of phosphate buffered saline. Five samples were then withdrawn from this solution and the The reproductive system of male birds comprises number of sperm counted under a microscopeusing the two testes and their connections to the cloaca via an Improved Neubauer counting chamber.Estimates the ductus deferens (see review in Lake 1981). The for both glomerawere summedto obtain an estimate distal end of each ductus deferens is known as the of total number of sperm stored.For comparativepur- seminal glomerusand, during the breeding season, poses,I also estimated the number of sperm in the it becomesexpanded and highly coiled,pushing out seminal glomera of one Lapland Longspur (C. lap- of the body cavity, and forming an externally visible ponicus),one American Tree Sparrow (Spizellaarborea), cloacal protuberancearound the vent (Wolfson 1952, and three Yellow-headed Blackbirds. All birds were October1993] ReproductiveAnatomy of Smith's Longspurs 877 TABLEI. Summaryof data on cloacal-protuberancedimensions (_+SE), testis lengths and samplesizes for