BMC Evolutionary Biology | |
Environmental quality alters female costs and benefits of evolving under enforced monogamy | |
Oliver Y Martin3  Matthew JG Gage2  Łukasz Michalczyk1  Marco Demont3  Vera M Grazer3  | |
[1] Department of Entomology, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland;School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, United Kingdom;ETH Zürich, Institute of Integrative Biology, D-USYS, Universitätsstrasse 16, CH-8092 Zürich, Switzerland | |
关键词: Reproductive success; Mating costs; Monogamy; Polyandry; Tribolium; Sexual conflict; | |
Others : 858035 DOI : 10.1186/1471-2148-14-21 |
|
received in 2013-09-24, accepted in 2014-01-30, 发布年份 2014 | |
【 摘 要 】
Background
Currently many habitats suffer from quality loss due to environmental change. As a consequence, evolutionary trajectories might shift due to environmental effects and potentially increase extinction risk of resident populations. Nevertheless, environmental variation has rarely been incorporated in studies of sexual selection and sexual conflict, although local environments and individuals’ condition undoubtedly influence costs and benefits. Here, we utilise polyandrous and monogamous selection lines of flour beetles, which evolved in presence or absence of sexual selection for 39 generations. We specifically investigated effects of low vs. standard food quality (i.e. stressful vs. benign environments) on reproductive success of cross pairs between beetles from the contrasting female and male selection histories to assess gender effects driving fitness.
Results
We found a clear interaction of food quality, male selection history and female selection history. Monogamous females generally performed more poorly than polyandrous counterparts, but reproductive success was shaped by selection history of their mates and environmental quality. When monogamous females were paired with polyandrous males in the standard benign environment, females seemed to incur costs, possibly due to sexual conflict. In contrast, in the novel stressful environment, monogamous females profited from mating with polyandrous males, indicating benefits of sexual selection outweigh costs.
Conclusions
Our findings suggest that costs and benefits of sexually selected adaptations in both sexes can be profoundly altered by environmental quality. With regard to understanding possible impacts of environmental change, our results further show that the ecology of mating systems and associated selection pressures should be considered in greater detail.
【 授权许可】
2014 Grazer et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140723092004153.pdf | 411KB | download | |
43KB | Image | download | |
55KB | Image | download |
【 图 表 】
【 参考文献 】
- [1]Jennions MD, Petrie M: Why do females mate multiply? A review of the genetic benefits. Biol Rev 2000, 75:21-64.
- [2]Neff BD, Pitcher TE: Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol Ecol 2005, 14:19-38.
- [3]Zeh JA, Zeh DW: Reproductive mode and the genetic benefits of polyandry. Anim Behav 2001, 61:1051-1063.
- [4]Zeh JA, Zeh DW: The evolution of polyandry I: intragenomic conflict and genetic incompatibility. Proc Roy Soc Lond B 1996, 263:1711-1717.
- [5]Zeh JA, Zeh DW: The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc Roy Soc Lond B 1997, 264:69-75.
- [6]Ewers RM, Didham RK: Confounding factors in the detection of species responses to habitat fragmentation. Biol Rev 2006, 81:117-142.
- [7]Bhattacharya M, Primack RB, Gerwein J: Are roads and railroads barriers to bumblebee movement in a temperate suburban conservation area? Biol Conserv 2003, 109:37-45.
- [8]Keller I, Nentwig W, Largiader CR: Recent habitat fragmentation due to roads can lead to significant genetic differentiation in an abundant flightless ground beetle. Mol Ecol 2004, 13:2983-2994.
- [9]Cushman SA: Effects of habitat loss and fragmentation on amphibians: a review and prospectus. Biol Conserv 2006, 128:231-240.
- [10]Travis JMJ: Climate change and habitat destruction: a deadly anthropogenic cocktail. Proc Roy Soc Lond B 2003, 270:467-473.
- [11]Bijlsma R, Bundgaard J, Boerema AC: Does inbreeding affect the extinction risk of small populations? Predictions from Drosophila. J Evol Biol 2000, 13:502-514.
- [12]Brook BW, Tonkyn DW, Q’Grady JJ, Frankham R: Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 2002, 6:16.
- [13]Wright LI, Tregenza T, Hosken DJ: Inbreeding, inbreeding depression and extinction. Conserv Genet 2008, 9:833-843.
- [14]Martin OY, Hosken DJ, Ward PI: Postcopulatory sexual selection and female fitness in Scathophaga stercoraria. Proc Roy Soc Lond B 2004, 271:353-359.
- [15]Banks SC, Piggott MP, Stow AJ, Taylor AC: Sex and sociality in a disconnected world: a review of the impacts of habitat fragmentation on animal social interactions. Can J Zool 2007, 85:1065-1079.
- [16]Sambatti JBM, Stahl E, Harrison S: Metapopulation structure and the conservation consequences of population fragmentation. In Conservation Biology: Evolution in Action. Edited by Carroll SP, Fox CW. New York: Oxford University Press; 2008:50-67.
- [17]Baer B, Schmid-Hempel P: Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 2001, 55:1639-1643.
- [18]Baer B, Schmid-Hempel P: Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 1999, 397:151-154.
- [19]Whitlock MC: Fixation of new alleles and the extinction of small populations: drift load, beneficial alleles, and sexual selection. Evolution 2000, 54:1855-1861.
- [20]Radwan J: Effectiveness of sexual selection in removing mutations induced with ionizing radiation. Ecol Lett 2004, 7:1149-1154.
- [21]Hollis B, Fierst JL, Houle D: Sexual selection accelerates the elimination of a deleterious mutant in Drosophila melanogaster. Evolution 2009, 63:324-333.
- [22]Tregenza T, Wedell N: Polyandrous females avoid costs of inbreeding. Nature 2002, 415:71-73.
- [23]Jarzebowska M, Radwan J: Sexual selection counteracts extinction of small populations of the bulb mites. Evolution 2010, 64:1283-1289.
- [24]Michalczyk Ł, Millard AL, Martin OY, Lumley AJ, Emerson BC, Chapman T, Gage MJG: Inbreeding promotes female promiscuity. Science 2011, 333:1739-1742.
- [25]Price TAR, Hurst GDD, Wedell N: Polyandry prevents extinction. Curr Biol 2010, 20:471-475.
- [26]Legendre S, Clobert J, Moller AP, Sorci G: Demographic stochasticity and social mating system in the process of extinction of small populations: the case of passerines introduced to New Zealand. Am Nat 1999, 153:449-463.
- [27]Sorci G, Moller AP, Clobert J: Plumage dichromatism of birds predicts introduction success in New Zealand. J Anim Ecol 1998, 67:263-269.
- [28]Kotiaho JS: Costs of sexual traits: a mismatch between theoretical considerations and empirical evidence. Biol Rev 2001, 76:365-376.
- [29]Twiss SD, Thomas C, Poland V, Graves JA, Pomeroy P: The impact of climatic variation on the opportunity for sexual selection. Biol Lett 2007, 3:12-15.
- [30]Candolin U, Salesto T, Evers M: Changed environmental conditions weaken sexual selection in sticklebacks. J Evol Biol 2007, 20:233-239.
- [31]Maan ME, Seehausen O, Van Alphen JJM: Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish. Biol J Linn Soc 2010, 99:398-406.
- [32]Botero CA, Rubenstein DR: Fluctuating environments, sexual selection and the evolution of flexible mate choice in birds. PLoS ONE 2012, 7:1-7.
- [33]Candolin U, Heuschele J: Is sexual selection beneficial during adaptation to environmental change? Trends Ecol Evol 2008, 23:446-452.
- [34]Ingleby FC, Hunt J, Hosken DJ: The role of genotype-by-environment interactions in sexual selection. J Evol Biol 2010, 23:2031-2045.
- [35]Greenfield MD, Rodriguez RL: Genotype-environment interaction and the reliability of mating signals. Anim Behav 2004, 68:1461-1468.
- [36]Bussière LF, Hunt J, Stolting KN, Jennions MD, Brooks R: Mate choice for genetic quality when environments vary: suggestions for empirical progress. Genetica 2008, 134:69-78.
- [37]Narraway C, Hunt J, Wedell N, Hosken DJ: Genotype-by-environment interactions for female preference. J Evol Biol 2010, 23:2550-2557.
- [38]Maan ME, Seehausen O: Ecology, sexual selection and speciation. Ecol Lett 2011, 14:591-602.
- [39]Tanaka Y: Sexual selection enhances population extinction in a changing environment. J Theor Biol 1996, 180:197-206.
- [40]Grazer VM, Martin OY: Investigating climate change and reproduction: Experimental tools from evolutionary biology. Biology 2012, 1:411-438.
- [41]Watson PJ, Arnqvist G, Stallmann RR: Sexual conflict and the energetic costs of mating and mate choice in water striders. Am Nat 1998, 151:46-58.
- [42]Blanckenhorn WU, Hosken DJ, Martin OY, Reim C, Teuschl Y, Ward PI: The costs of copulating in the dung fly Sepsis cynipsea. Behav Ecol 2002, 13:353-358.
- [43]Wigby S, Chapman T: Sex peptide causes mating costs in female Drosophila melanogaster. Curr Biol 2005, 15:316-321.
- [44]Demont M, Grazer VM, Michalczyk L, Millard AL, Sbilordo SH, Emerson BC, Gage MJG, Martin OY: Experimental removal of sexual selection reveals adaptations to polyandry in both sexes. Evol BiolIn press
- [45]Michalczyk Ł, Millard AL, Martin OY, Lumley AJ, Emerson BC, Gage MJG: Experimental evolution exposes female and male responses to sexual selection and conflict in Tribolium castaneum. Evolution 2011, 65:713-724.
- [46]Cahill AE, Aiello-Lammens ME, Fisher-Reid MC, Hua X, Karanewsky CJ, Ryu HY, Gena C, Sbeglia GC, Spagnolo F, Waldron JB, Warsi O, Wiens JJ, Proc Roy Soc Lond B: How does climate change cause extinction? Proc Roy Soc Lond 2013, 280:1750-20121890.
- [47]Sbilordo SH, Grazer VM, Demont M, Martin OY: Impacts of starvation on male reproductive success in Tribolium castaneum. Evol Ecol Res 2011, 13:347-359.
- [48]Lewis SM, Tigreros N, Fedina T, Ming QL: Genetic and nutritional effects on male traits and reproductive performance in Tribolium flour beetles. J Evol Biol 2012, 25:438-451.
- [49]Kerstes NAG, Bérénos C, Martin OY: Coevolving parasites and population size shape the evolution of mating behaviour. BMC Evol Biol 2013, 13:29. BioMed Central Full Text
- [50]Grazer VM, Martin OY: Elevated temperature changes female costs and benefits of reproduction. Evol Ecol 2012, 26:625-637.
- [51]Sokoloff A, Franklin IR, Overton LF, Ho FK: Comparative studies with Tribolium (Coleoptera, Tenebrionidae) - I: Productivity of T. castaneum (Herbst) and T. confusum Duv. on several commercially-available diets. J Stored Prod Res 1966, 1:295-311.
- [52]Fricke C, Perry J, Chapman T, Rowe L: The conditional economics of sexual conflict. Biol Lett 2009, 5:671-674.
- [53]Creighton JC, Heflin ND, Belk MC: Cost of reproduction, resource quality, and terminal investment in a burying beetle. Am Nat 2009, 174:673-684.
- [54]Roff DA: Life History Evolution. Sunderland: Sinauer Associates; 2002.
- [55]Stearns SC: Trade-offs in life-history evolution. Funct Ecol 1989, 3:259-268.
- [56]Marshall KE, Sinclair BJ: Repeated stress exposure results in a survival-reproduction trade-off in Drosophila melanogaster. Proc Roy Soc Lond B 2010, 277:963-969.
- [57]Hosken DJ, Garner TWJ, Ward PI: Sexual conflict selects for male and female reproductive characters. Curr Biol 2001, 11:489-493.
- [58]Hosken DJ, Ward PI: Experimental evidence for testis size evolution via sperm competition. Ecol Lett 2001, 4:10-13.
- [59]Pitnick S, Miller GT, Reagan J, Holland B: Males’ evolutionary responses to experimental removal of sexual selection. Proc Roy Soc Lond B 2001, 268:1071-1080.
- [60]Simmons LW, Garcia-Gonzalez F: Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution 2008, 62:2580-2591.
- [61]Crudgington HS, Beckerman AP, Brüstle L, Green K, Snook RR: Experimental removal and elevation of sexual selection: does sexual selection generate manipulative males and resistant females? Am Nat 2005, 165:S72-S87.
- [62]Martin OY, Hosken DJ: Costs and benefits of evolving under experimentally enforced polyandry or monogamy. Evolution 2003, 57:2765-2772.
- [63]Hellriegel B, Blanckenhorn WU: Environmental influences on the gametic investment of yellow dung fly males. Evol Ecol 2002, 16:505-522.
- [64]Spratt EC: Male homosexual behaviour and other factors influencing adult longevity in Tribolium castaneum (Herbst) and T. confusum Duval. J Stored Prod Res 1980, 16:109-114.
- [65]Sokoloff A: The Biology of Tribolium with Special Emphasis on Genetic Aspects. Oxford: Oxford University Press; 1972.
- [66]Long TAF, Agrawal A, Rowe L: The effect of sexual selection on offspring fitness depends on the nature of genetic variation. Curr Biol 2012, 22:204-208.
- [67]Dudash MR, Murren CJ: The influence of breeding systems and mating systems on conservation genetics and conservation decisions. In Conservation Biology: Evolution in Action. Edited by Carroll SP, Fox CW. New York: Oxford University Press; 2008:68-80.