Stepping off the pasture: evidence of widespread alternative male mating tactics in the yellow dung fly

in Behaviour
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Geoff Parker’s investigations of the yellow dung fly mating system revitalized interest in sexual selection theory, sparked development of sperm competition and sexual conflict theories, and stimulated use of this species as an important model system. Numerous studies across widespread populations have demonstrated large-male advantages in competition contests occurring on dung in cow pastures; however, recent work suggests that smaller males adopt an alternative mating tactic by avoiding dung and instead copulating with females at foraging sites. Though this finding has the potential to expand our understanding of sexual selection in yellow dung flies, such behavior has to date been documented at only one field site, raising the possibility that this phenomenon is highly localized. Here, we report the expression of size-dependent alternative mating tactics across three discrete populations. These findings provide a cautionary tale for researchers limiting their attention to aggregation sites where study organisms are most conveniently encountered.

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References

AmanoK. (1983). Studies on the intraspecific competition in dung-breeding flies. I. Effects of larval density on yellow dung fly, Scatophaga stercoraria L. (Diptera: Scatophagidae). — Jpn. J. Sanit Zool. 34: 165-175.

BenningtonC.C.McGrawJ.B. (1995). Phenotypic selection in an artificial population of Impatiens pallida: the importance of the invisible fraction. — Evolution 49: 317-324.

BirkheadT.R.MonaghanP. (2010). Ingenious ideas: the history of behavioral ecology. — In: Evolutionary behavioral ecology ( WestneatD.F.FoxC.W., eds). Oxford University Press, Oxford, p.  3-15.

BirkheadT.R.MontgomerieR. (2009). Three centuries of sperm research. — In: Sperm biology: an evolutionary perspective ( BirkheadT.R.HoskenD.J.PitnickS., eds). Academic Press, New York, NY, p.  1-42.

BlanckenhornW.U. (1997). Effects of temperature on growth, development and diapause in the yellow dung fly — against all the rules?Oecologia 111: 318-324.

BlanckenhornW.U. (1998). Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly. — Evolution 52: 1394-1407.

BlanckenhornW.U.FreiJ.BirrerM. (2003). The effect of female arrivals on mate monopolization in the yellow dung fly. — Behav. Ecol. Sociobiol. 54: 65-70.

BlanckenhornW.U.PembertonA.J.BussièreL.F.RoembkeJ.FloateK.D. (2010). A review of the natural history and laboratory culture methods for the yellow dung fly, Scathophaga stercoraria. — J. Insect Sci. 10: 1-17.

BorgiaG. (1980). Sexual competition in Scatophaga stercoraria: size- and density-related changes in male ability to capture females. — Behaviour 75: 185-206.

BorgiaG. (1981). Mate selection in the fly Scatophaga stercoraria: female choice in a male-controlled system. — Anim. Behav. 29: 71-80.

BussièreL.F.DemontM.PembertonA.J.HallM.D.WardP.I. (2010). The assessment of insemination success in yellow dung flies using competitive PCR. — Mol. Ecol. 10: 292-303.

CarrollS.P. (1993). Divergence in male mating tactics between two populations of the soapberry bug: I. Guarding versus nonguarding. — Behav. Ecol. 4: 156-164.

CarrollS.P.CorneliP.S. (1995). Divergence in male mating tactics between two populations of the soapberry bug: II. Genetic change and the evolution of a plastic reaction norm in a variable social environment. — Behav. Ecol. 6: 46-56.

CharnovE.L. (1976). Optimal foraging, the marginal value theorem. — Theor. Popul. Biol. 9: 129-136.

DemontM.BlanckenhornW.U.HoskenD.J.GarnerT.W.J. (2008). Molecular and quantitative genetic differentiation across Europe in yellow dung flies. — J. Evol. Biol. 21: 1492-1503.

DingA.BlanckenhornW.U. (2002). The effect of sexual size dimorphism on mating behaviour in two dung flies with contrasting dimorphism. — Evol. Ecol. Res. 4: 259-273.

FretwellS.D. (1972). Populations in a seasonal environment. — Princeton University Press, Princeton.

FretwellS.D.LucasH.L.Jr. (1970). On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. — Acta Biotheor. 19: 16-36.

GodinJ.-G.J. (1995). Predation risk and alternative mating tactics in male Trinidadian guppies (Poecilia reticulata). — Oecologia 103: 224-229.

GressB.E.WaltzerR.J.LüpoldS.Droge-YoungE.M.ManierM.K.PitnickS. (2014). Alternative mating tactics in the yellow dung fly: resolving mechanisms of small-male advantage off pasture. — Proc. Roy. Soc. Lond. B: Biol. Sci. 281: 20132164.

GrossM.R. (1996). Alternative reproductive strategies and tactics: diversity within sexes. — Trends Ecol. Evol. 11: 92-98.

HadfieldJ.D. (2008). Estimating evolutionary parameters when viability selection is operating. — Proc. Roy. Soc. Lond. B: Biol. Sci. 275: 723-734.

HoskenD.J.BlanckenhornW.U.GarnerT.W.J. (2002). Heteropopulation males have a fertilization advantage during sperm competition in the yellow dung fly (Scathophaga stercoraria). — Proc. Roy. Soc. Lond. B: Biol. Sci. 269: 1701-1707.

JannP.BlanckenhornW.U.WardP.I. (2000). Temporal and microspatial variation in the intensities of natural and sexual selection in the yellow dung fly Scathophaga stercoraria. — J. Evol. Biol. 13: 927-938.

KolluruG.R.GretherG.F. (2005). The effects of resource availability on alternative mating tactics in guppies (Pecilia reticulata). — Behav. Ecol. 16: 294-300.

LivelyC.M. (1986). Canalization versus developmental conversion in a spatially variable environment. — Am. Nat. 218: 561-572.

OliveiraR.SchlindweinC. (2010). Experimental demonstration of alternative mating tactics of male Ptilothrix fructifera (Hymenoptera, Apidae). — Anim. Behav. 80: 241-247.

OtronenM. (1995). Energy reserves and mating success in males of the yellow dung fly, Scathophaga stercoraria. — Funct. Ecol. 9: 683-688.

OtronenM.RegueraP.WardP.I. (1997). Sperm storage in the yellow dung fly Scathophaga stercoraria: identifying the sperm of competing males in separate female spermathecae. — Ethology 103: 844-854.

ParkerG.A. (1970a). Sperm competition and its evolutionary consequences in the insects. — Biol. Rev. 45: 525-567.

ParkerG.A. (1970b). Sperm competition and its evolutionary effect on copula duration in the fly Scatophaga stercoraria. — J. Insect Physiol. 16: 1301-1328.

ParkerG.A. (1970c). The reproductive behavior and the nature of sexual selection in Scatophaga stercoraria L. (Diptera: Scatophagidae). VII. The origin and evolution of the passive phase. — Evolution 24: 774-788.

ParkerG.A. (1970d). The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. (Diptera: Scatophagidae): I. Diurnal and seasonal changes in population density around the site of mating and oviposition. — J. Anim. Ecol. 39: 185-204.

ParkerG.A. (1970e). The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. (Diptera: Scatophagidae): II. The fertilization rate and the spatial and temporal relationships of each sex around the site of mating and oviposition. — J. Anim. Ecol. 39: 205-228.

ParkerG.A. (1970f). The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. (Diptera: Scatophagidae). V. The female’s behaviour at the oviposition site. — Behaviour 37: 140-168.

ParkerG.A. (1971). The reproductive behaviour and the nature of sexual selection in Scatophaga stercoraria L. (Diptera: Scatophagidae). VI. The adaptive significance of emigration from the oviposition site during the phase of genital contact. — J. Anim. Ecol. 40: 215-233.

ParkerG.A. (1979). Sexual selection and sexual conflict. — In: Sexual selection and reproductive competition in insects ( BlumM.S.BlumN.A., eds). Academic Press, New York, NY, p.  123-166.

ParkerG.A. (1990). Sperm competition games: raffles and roles. — Proc. Roy. Soc. Lond. B: Biol. Sci. 242: 120-126.

ParkerG.A. (1992). Marginal value theorem with exploitation time costs: diet, sperm reserves, and optimal copula duration in dung flies. — Am. Nat. 139: 1237-1256.

ParkerG.A. (2001). Golden flies, sunlit meadows: a tribute to the yellow dungfly. — In: Model systems in behavioral ecology: integrating conceptual, theoretical, and empirical approaches ( DugatkinL.A., ed.). Princeton University Press, Princeton, NJ, p.  3-26.

ParkerG.A. (2006). Behavioural ecology: natural history as science. — In: Essays in Animal Behaviour: celebrating 50 years of Animal Behaviour ( LucasJ.R.SimmonsL.W., eds). Elsevier, London, p.  23-56.

ParkerG.A.StuartR.A. (1976). Animal behavior as a strategy optimizer: evolution of resource assessment strategies and optimal emigration thresholds. — Am. Nat. 110: 1055-1076.

ParkerG.A.SimmonsL.W.WardP.I. (1993). Optimal copula duration in dungflies: effects of frequency dependence and female mating status. — Behav. Ecol. Sociobiol. 32: 157-166.

PichéJ.HutchingsJ.A.BlanchardW. (2008). Genetic variation in threshold reaction norm for alternative reproductive tactics in male Atlantic salmon, Salmo salar. — Proc. Roy. Soc. Lond. B: Biol. Sci. 275: 1571-1575.

PitnickS.HennK.R.H.MaheuxS.D.HigginsonD.M.Hurtado-GonzalesJ.L.ManierM.K.BerbenK.S.GuptillC.UyJ.A.C. (2009). Size-dependent alternative male mating tactics in the yellow dung fly, Scathophaga stercoraria. — Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 3229-3237.

R Development Core Team (2015). R: a language and environment for statistical computing. — R Foundation for Statistical Computing, Vienna.

ShaliniR.GuptaD.K. (2010). Utilization of pomace from apple processing industries: a review. — J. Food Sci. Technol. 47: 365-371.

SigurjónsdóttirH.ParkerG.A. (1981). Dung fly struggles: evidence for assessment strategy. — Behav. Ecol. Sociobiol. 8: 219-230.

SigurjónsdóttirH.SnorrasonS.S. (1995). Distribution of male yellow dungflies around ovipasition sites: the effect of body size. — Ecol. Entomol. 20: 84-90.

SimmonsL.W.WardP.I. (1991). The heritability of sexually dimorphic traits in the yellow dung fly Scathophaga stercoraria (L.). — J. Evol. Biol. 4: 593-601.

SinervoB.McAdamA.G. (2008). Maturational costs of reproduction due to clutch size and ontogenetic conflict as revealed in the invisible fraction. — Proc. Roy. Soc. Lond. B: Biol. Sci. 275: 629-638.

SmithJ.M.ParkerG.A. (1976). The logic of asymmetric contests. — Anim. Behav. 24: 159-175.

TomkinsJ.L.BrownG.S. (2004). Population density drives the local evolution of a threshold dimorphism. — Nature 431: 1099-1103.

USDA (2014). 2014 Washington annual statistical bulletin. — United States Department of Agriculture, Washington, DC.

SigurjónsdóttirH.SnorrasonS.S. (1995). Distribution of male yellow dungflies around ovipasition sites: the effect of body size. — Ecol. Entomol. 20: 84-90.

PitnickS.HennK.R.H.MaheuxS.D.HigginsonD.M.Hurtado-GonzalesJ.L.ManierM.K.BerbenK.S.GuptillC.UyJ.A.C. (2009). Size-dependent alternative male mating tactics in the yellow dung fly, Scathophaga stercoraria. — Proc. Roy. Soc. Lond. B: Biol. Sci. 276: 3229-3237.

SAS Institute (2014). SAS software. — SAS Institute, Cary, NC.

Figures

  • (a) Experimental mesocosm pasture constructed in the greenhouse on Syracuse University’s campus, and S. stercoraria within mesocosms, (b) copulating on pomace, (c) copulating on dung and (d) two males grappling over possession of a female on dung. This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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  • Mean hind tibia length (HTL) for copulating males on dung (CD; N=280), copulating males on pomace (CP; N=34), single males on dung (SD; N=517), and single males on pomace (SP; N=33) collected in the field. Error bars represent 95% confidence intervals.

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  • Predicted probability curves representing the likelihood that a male of a given size (HTL) adopts the competitor tactic for each population. NY, solid line; WA, short dashed line; CA, long dashed line.

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