Abstract
Many studies that have researched interspecific competition in Callosobruchus (bean beetles), Drosophila (fruit flies), and Tribolium (flour beetles) have considered the major drivers of interspecific competition to be interspecific resource competition and intraguild cannibalism. These competition drivers have a density-dependent effect on the population dynamics. However, some studies have also detected a relative-frequency-dependent effect in the observed population dynamics. The most likely causal mechanism of this relative frequency dependence is reproductive interference, defined as any interspecific sexual interaction that damages female reproductive success. Reproductive interference has been overlooked by most laboratory studies in spite of the critical effect on the competition outcome. In this paper, I review laboratory studies of these insect genera from the perspective of reproductive interference and show that the reported results can be more reasonably interpreted by the joint action of reproductive interference and resource competition, including intraguild cannibalism. In addition, on the basis of results reported by a small number of related studies, I discuss the behavioral and evolutionary changes induced in those genera by reproductive interference.
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References
Aiken RB, Gibo DL (1979) Changes in fecundity of Drosophila melanogaster and D. simulans in response to selection for competitive ability. Oecologia 43:63–77
Amézquita A, Hödl W, Lima AP, Castellanos L, Erdtmann L, Araújo MC (2006) Masking interference and the evolution of the acoustic communication system in the Amazonian dendrobatid frog Allobates femoralis. Evolution 60:1874–1887
Amézquita A, Flechas SV, Lima AP, Gasser H, Hödl W (2011) Acoustic interference and recognition space within a complex assemblage of dendrobatid frogs. Proc Natl Acad Sci USA 108:17058–17063
Antonovics J, Kareiva P (1988) Frequency-dependent selection and competition: empirical approaches. Philos Trans R Soc Lond B Biol Sci 319:601–613
Arnqvist G, Tuda M (2010) Sexual conflict and the gender load: correlated evolution between population fitness and sexual dimorphism in seed beetles. Proc R Soc B 277:1345–1352
Ayala FJ (1971) Competition between species: frequency dependence. Science 171:820–824
Ayala FJ, Campbell CA (1974) Frequency-dependent selection. Ann Rev Ecol Syst 5:115–138
Ayala FJ, Gilpin ME, Ehrenfeld JG (1973) Competition between species: theoretical models and experimental tests. Theor Popul Biol 4:331–356
Barker JSF (1963) The estimation of relative fitness of Drosophila populations. III. The fitness of certain strains of Drosophila melanogaster. Evolution 17:138–146
Barker JSF (1971) Ecological differences and competitive interaction between Drosophila melanogaster and Drosophila simulans in small laboratory populations. Oecologia 8:139–156
Barker JSF, Podger RN (1970) Interspecific competition between Drosophila melanogaster and Drosophila simulans: effects of larval density on viability, developmental period and adult body weight. Ecology 51:170–189
Begon M, Townsend CR, Harper JL (2009) Ecology: from individuals to ecosystems, 4th edn. Blackwell Publishing, Malden
Bellows TS, Hassell MP (1984) Models for interspecific competition in laboratory populations of Callosobruchus spp. J Anim Ecol 53:831–848
Birch LC, Park T, Frank MB (1951) The effect of intraspecies and interspecies competition on the fecundity of two species of flour beetles. Evolution 5:116–132
Budnik M, Brncic D (1974) Preadult competition between Drosophila pavani and Drosophila melanogaster, Drosophila simulans, and Drosophila willistoni. Ecology 55:657–661
Cain ML, Bowman WD, Hacker SD (2008) Ecology. Sinauer Associates, Sunderland
Chess KF, Ringo JM, Dowse HB (1990) Oviposition by two species of Drosophila (Diptera: Drosophilidae): behavioral responses to resource distribution and competition. Ann Entomol Soc Am 83:717–724
Crenshaw JW (1966) Productivity and competitive ability in Tribolium. Am Nat 100:683–687
Crombie AC (1947) Interspecific competition. J Anim Ecol 16:44–73
Crudgington HS, Siva-Jothy MT (2000) Genital damage, kicking and early death. Nature 407:855–856
Dawson PS (1966) Developmental rate and competitive ability in Tribolium. Evolution 20:104–116
Dawson PS (1967) Developmental rate and competitive ability in Tribolium—III: competition in unfavorable environments. J Stored Prod Res 3:193–198
Dawson PS (1970) A further assessment of the role of founder effects in the outcome of Tribolium competition experiments. Proc Natl Acad Sci USA 66:1112–1118
Dawson PS (1977) Life history strategy and evolutionary history of Tribolium flour beetles. Evolution 31:226–229
Dawson PS (1979) Evolutionary changes in egg-eating behavior of flour beetles in mixed-species populations. Evolution 33:585–594
Dawson PS, Lerner IM (1966) The founder principle and competitive ability of Tribolium. Proc Natl Acad Sci USA 55:1114–1117
DeBenedictis PA (1977) The meaning and measurement of frequency-dependent competition. Ecology 58:158–166
Dobzhansky T (1943) Genetics of natural populations IX. Temporal changes in the composition of populations of Drosophila pseudoobscura. Genetics 28:162–186
Dukas R (2004) Male fruit flies learn to avoid interspecific courtship. Behav Ecol 15:695–698
Eady PE, Hamilton L, Lyons RE (2007) Copulation, genital damage and early death in Callosobruchus maculatus. Proc R Soc B 274:247–252
Edmunds J, Cushing JM, Costantino RF, Henson SM, Dennis B, Desharnais RA (2003) Park’s Tribolium competition experiments: a non-equilibrium species coexistence hypothesis. J Anim Ecol 72:703–712
Eoff M (1975) Artificial selection in Drosophila melanogaster females for increased and decreased sexual isolation from D. simulans males. Am Nat 109:225–229
Ewing AW (1983) Functional aspects of Drosophila courtship. Biol Rev 58:275–292
Ewing AW, Bennet-Clark HC (1968) The courtship songs of Drosophila. Behaviour 31:288–301
Fedina TY, Lewis SM (2008) An integrative view of sexual selection in Tribolium flour beetles. Biol Rev 83:151–171
Fox CW, Stillwell RC, Wallin WG, Hitchcock LJ (2006) Temperature and host species affect nuptial gift size in a seed-feeding beetle. Funct Ecol 20:1003–1011
Fujii K (1965) Studies on interspecies competition between the azuki bean weevil and the southern cowpea weevil. Res Popul Ecol 7:43–51
Fujii K (1967) Studies on interspecies competition between the azuki bean weevil, Callosobruchus chinensis, and the southern cowpea weevil, C. maculatus II. Competition under different environmental conditions. Res Popul Ecol 9:192–200
Fujii K (1968) Studies on interspecies competition between the azuki bean weevil and the southern cowpea weevil. III. Some characteristics of strains of two species. Res Popul Ecol 10:87–98
Fujii K (1969) Studies on the interspecies competition between the azuki bean weevil and the southern cowpea weevil IV. Competition between strains. Res Popul Ecol 11:84–91
Fujii K (1970) Studies on the interspecies competition between the azuki bean weevil, Callosobruchus chinensis, and the southern cowpea weevil, C. maculatus V. The role of adult behavior in competition. Res Popul Ecol 12:233–242
Fujita H, Utida S (1953) The effect of population density on the growth of an animal population. Ecology 34:488–498
Gause GF (1934) The struggle for existence. Baltimore, Williams and Wilkins
Ghent AW (1963) Studies of behavior of the Tribolium flour beetles. I. Contrasting responses of T. castaneum and T. confusum to fresh and conditioned flours. Ecology 44:269–283
Ghent AW (1966) Studies of behavior of the Tribolium flour beetles. II. Distributions in depth of T. castaneum and T. confusum in fractionable shell vials. Ecology 47:355–367
Goodnight CJ, Craig DM (1996) The effect of coexistence on competitive outcome in Tribolium castaneum and Tribolium confusum. Evolution 50:1241–1250
Graur D, Wool D (1985) Undirectional interspecific mating in Tribolium castaneum and T. confusum: evolutionary and ecological implications. Entomol Exp Appl 38:261–265
Greenspan RJ, Ferveur JF (2000) Courtship in Drosophila. Ann Rev Genet 34:205–232
Gröning J, Hochkirch A (2008) Reproductive interference between animal species. Q Rev Biol 83:257–282
Harano T, Miyatake T (2005) Heritable variation in polyandry in Callosobruchus chinensis. Anim Behav 70:299–304
Harano T, Miyatake T (2007) Interpopulation variation in female remating is attributable to female and male effects in Callosobruchus chinensis. J Ethol 25:49–55
Hassell MP (1975) Density-dependence in single-species populations. J Anim Ecol 44:283–295
Hedrick PW (1972) Factors responsible for a change in interspecific competitive ability in Drosophila. Evolution 26:513–522
Hochkirch A, Gröning J, Bücker A (2007) Sympatry with the devil: reproductive interference could hamper species coexistence. J Anim Ecol 76:633–642
Hotta Y, Okada M (1989) Developmental genetics of Drosophila. Maruzen, Tokyo
Inouye N, Lerner IM (1965) Competition between Tribolium species (Coleoptera, Tenebrionidae) on several diets. J Stored Prod Res 1:185–191
Ishii Y, Shimada M (2008) Competitive exclusion between contest and scramble strategists in Callosobruchus seed–beetle modeling. Popul Ecol 50:197–205
Izquierdo JI, Carracedo MC, Piñeiro R, Casares P (1992) Response to selection for increased hybridization between Drosophila melanogaster females and D. simulans males. J Hered 83:100–104
Katsuki M, Miyatake T (2009) Effects of temperature on mating duration, sperm transfer and remating frequency in Callosobruchus chinensis. J Insect Physiol 55:113–116
Katsuki M, Toquenaga Y, Miyatake T (2013) Larval competition causes the difference in male ejaculate expenditure in Callosobruchus maculatus. Popul Ecol 55:493–498
Kawanishi M, Watanabe TK (1981) Genes affecting courtship song and mating preference in Drosophila melanogaster, Drosophila simulans and their hybrids. Evolution 35:1128–1133
Kishi S, Nakazawa T (2013) Analysis of species coexistence co-mediated by resource competition and reproductive interference. Popul Ecol 55:305–313
Kishi S, Tsubaki Y (2014) Avoidance of reproductive interference causes resource partitioning in bean beetle females. Popul Ecol 56:73–80
Kishi S, Nishida T, Tsubaki Y (2009) Reproductive interference determines persistence and exclusion in species interactions. J Anim Ecol 78:1043–1049
Kuno E (1992) Competitive exclusion through reproductive interference. Res Popul Ecol 34:275–284
Kuno E, Kozai Y, Kubotsu K (1995) Modelling and analyzing density-dependent population processes: comparison between wild and laboratory strains of the bean weevil, Callosobruchus chinensis (L.). Res Popul Ecol 37:165–176
Kyogoku D, Nishida T (2012) The presence of heterospecific males causes an Allee effect. Popul Ecol 54:391–395
Kyogoku D, Nishida T (2013) The mechanism of the fecundity reduction in Callosobruchus maculatus caused by Callosobruchus chinensis males. Popul Ecol 55:87–93
Leslie PH, Park T, Mertz DB (1968) The effect of varying the initial numbers on the outcome of competition between two Tribolium species. J Anim Ecol 37:9–23
Lloyd M, Park T (1962) Mortality resulting from interactions between adult flour beetles in laboratory cultures. Physiol Zool 35:330–347
Lotka AJ (1924) Elements of physical biology. Dover Publishers, NY
Manning A (1959) The sexual isolation between Drosophila melanogaster and Drosophila simulans. Anim Behav 7:60–65
Markow TA (1981) Courtship behavior and control of reproductive isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 35:1022–1026
Merrell DJ (1951) Interspecific competition between Drosophila funebris and Drosophila melanogaster. Am Nat 85:159–169
Mertz DB, Cawthon DA, Park T (1976) An experimental analysis of competitive indeterminacy in Tribolium. Proc Natl Acad Soc USA 73:1368–1372
Miller RS (1964) Larval competition in Drosophila melanogaster and D. simulans. Ecology 45:132–148
Miyatake T, Matsumura F (2004) Intra-specific variation in female remating in Callosobruchus chinensis and C. maculatus. J Insect Physiol 50:403–408
Moore JA (1952) Competition between Drosophila melanogaster and Drosophila simulans. Proc Natl Acad Sci USA 38:813–817
Morgan TH (1910) The method of inheritance of two sex-limited characters in the same animal. Exp Biol Med 8:17–19
Moth JJ (1974) Density, frequency and interspecific competition: fertility of Drosophila simulans and Drosophila melanogaster. Oecologia 14:237–246
Moth JJ, Barker JSF (1977) Interspecific competition between Drosophila melanogaster and Drosophila simulans: effects of adult density on adult viability. Genetica 47:203–218
Moth JJ, Barker JSF (1981) Interspecific competition between Drosophila melanogaster and Drosophila simulans: effects of adult density, species frequency, light, and dietary phosphorus-32 on fecundity. Physiol Zool 54:28–43
Nagayasu M, Matsushita K (1981) Faunal survey of bean weevils in bean processing mills. Res Bull Pl Prot Jpn 17:87–91 (in Japanese)
Narise T (1965) The effect of relative frequency of species in competition. Evolution 19:350–354
Neyman J, Park T, Scott EL (1956) Struggle for existence. The Tribolium model: biological and statistical aspects. In: Proceedings of the Third Berkeley Symposium on Mathematical Statistics and Probability vol. 4. University of California Press, California, pp 41–79
Nunney L (1983) Sex differences in larval competition in Drosophila melanogaster: the testing of a competition model and its relevance to frequency-dependent selection. Am Nat 121:67–93
Park T (1934) Observations on the general biology of the flour beetle, Tribolium confusum. Q Rev Biol 9:36–54
Park T (1948) Interspecies competition in populations of Tribolium confusum Duval and Tribolium castaneum Herbst. Ecol Monogr 18:265–307
Park T (1954) Experimental studies of interspecies competition II. Temperature, humidity, and competition in two species of Tribolium. Physiol Zool 27:177–238
Park T, Mertz DB, Petrusewicz K (1961) Genetic strains of Tribolium: their primary characteristics. Physiol Zool 34:62–80
Park T, Leslie PH, Mertz DB (1964) Genetic strains and competition in populations of Tribolium. Physiol Zool 37:97–162
Park T, Mertz DB, Grodzinski W, Prus T (1965) Cannibalistic predation in populations of flour beetles. Physiol Zool 38:289–321
Park T, Nathanson M, Ziegler JR, Mertz DB (1970) Cannibalism of pupae by mixed-species populations of adult Tribolium. Physiol Zool 43:166–184
Park T, Ziegler JR, Ziegler DL, Mertz DB (1974) The cannibalism of eggs by Tribolium larvae. Physiol Zool 47:37–58
Pascual M, Sagarra E, Serra L (2000) Interspecific competition in the laboratory between Drosophila subobscura and D. azteca. Am Midl Nat 144:19–27
Post JR, Parkinson EA, Johnston NT (1999) Density-dependent processes in structured fish populations: interaction strengths in whole-lake experiments. Ecol Monogr 69:155–175
Powell JR (1997) Progress and prospects in evolutionary biology: The drosophila model. Oxford University Press, Oxford
Putwain PD, Antonovics J, Machin D (1967) The effect of relative frequency of species in competition: a reappraisal. Evolution 21:638–641
Reznick D, Bryant MJ, Bashey F (2002) r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83:1509–1520
Ribeiro JMC, Spielman A (1986) The satyr effect: a model predicting parapatry and species extinction. Am Nat 128:513–528
Rich ER (1956) Egg cannibalism and fecundity in Tribolium. Ecology 37:109–120
Rönn J, Katvala M, Arnqvist G (2006) The costs of mating and egg production in Callosobruchus seed beetles. Anim Behav 72:335–342
Sakurai G, Himuro C, Kasuya E (2012) Intra-specific variation in the morphology and the benefit of large genital sclerites of males in the adzuki bean beetle (Callosobruchus chinensis). J Evol Biol 25:1291–1297
Schoener TW (1983) Field experiments on interspecific competition. Am Nat 122:240–285
Serrano JM, Castro L, Toro MA, López-Fanjul C (2000) Inter- and intraspecific sexual discrimination in the flour beetles Tribolium castaneum and Tribolium confusum. Heredity 85:142–146
Sokoloff A (1972) The biology of Tribolium. Clarendon press, Oxford
Sokoloff A, Lerner IM (1967) Laboratory ecology and mutual predation of Tribolium species. Am Nat 101:261–276
Spieth HT (1974) Courtship behavior in Drosophila. Ann Rev Entomol 19:385–405
Takano M, Toquenaga Y, Fujii K (2001) Polymorphism of competition type and its genetics in Callosobruchus maculatus (Coleoptera: Bruchidae). Popul Ecol 43:265–273
Tantawy AO, Soliman MH (1967) Studies on natural populations of Drosophila VI. Competition between Drosophila melanogaster and Drosophila simulans. Evolution 21:34–40
Toquenaga Y (1993) Contest and scramble competitions in Callosobruchus maculatus (Coleoptera: Bruchidae) II. Larval competition and interference mechanisms. Res Popul Ecol 35:57–68
Tuda M (1998) Evolutionary character changes and population responses in an insect host-parasitoid experimental system. Res Popul Ecol 40:293–299
Umeya K (1987) Biology of bruchid beetles. Tsukiji Shokan, Tokyo
Utida S (1941) Studies on experimental population of the azuki bean weevil. I. The effect of population density on the progeny population. Mem Coll Agr Kyoto Imp Univ 48:1–30
Utida S (1950) On the equilibrium state of the interacting population of an insect and its parasite. Ecology 31:165–175
Utida S (1953) Interspecific competition between two species of bean weevil. Ecology 34:301–307
Utida S (1955) Fluctuations in the interacting populations of host and parasite in relation to the biotic potential of the host. Ecology 36:202–206
Utida S (1971) Influence of temperature on the number of eggs, mortality and development of several species of Bruchid infesting stored beans. Jpn J Appl Entomol Zool 15:23–30 (in Japanese)
Utida S (1998) Ecology of animal populations. Kyoto University Press, Kyoto
Verheggen F, Ryne C, Olsson P-OC, Arnaud L, Lognay G, Högberg HE, Persson D, Haubruge E, Löfstedt C (2007) Electrophysiological and behavioral activity of secondary metabolites in the confused flour beetle, Tribolium confusum. J Chem Ecol 33:525–539
Wallace B (1974) Studies on intra- and inter-specific competition in Drosophila. Ecology 55:227–244
Wasserman M, Koepfer HR (1977) Character displacement for sexual isolation between Drosophila mojavensis and Drosophila arizonensis. Evolution 31:812–823
Wood D, Ringo JM (1980) Male mating discrimination in Drosophila melanogaster. D. simulans and their hybrids. Evolution 34:320–329
Yoshida T (1957) Experimental studies on the interspecific competition among the granary beetles. No. 4. Competition between the azuki bean weevil, Callosobruchus chinensis and the southern cowpea weevil, C. quadrimaculatus. Mem Fac Lib Arts Educ Miyazaki Univ 61:55–80 (in Japanese with English summary)
Yoshida T (1958) The origin and root of stored product pests. Seibutsu Kagaku 10:60–68 (in Japanese)
Yoshida T (1966) Studies on the interspecific competition between bean weevils. Mem Fac Lib Arts Educ Miyazaki Univ 20:59–98
Yoshimura J, Clark CW (1994) Population dynamics of sexual and resource competition. Theor Popul Biol 45:121–131
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I thank Takayoshi Nishida, Koh-Ichi Takakura, Suzuki Noriyuki, and Daisuke Kyogoku for valuable discussions.
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Kishi, S. Reproductive interference in laboratory experiments of interspecific competition. Popul Ecol 57, 283–292 (2015). https://doi.org/10.1007/s10144-014-0455-0
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DOI: https://doi.org/10.1007/s10144-014-0455-0