Abstract
If natural selection on fluctuating asymmetry (FA) is common and related to trait functionality, then vestigial traits should show elevated FA. Moreover, if FA increases with heterozygosity, then haploid males of haplodiploid taxa should exhibit higher FA than diploid females. We measured fluctuating asymmetry of functional traits (fore femora of soldier morphs and disperser morphs, and wings of dispersers) and a vestigial trait (wings of soldiers) in the eusocial haplodiploid gall thrips Oncothrips tepperi (Insecta: Thysanoptera). Wing FA, but not femur FA, was substantially and significantly higher in soldiers than in dispersers in both sexes. Patterns of intersexual variation in FA were complex: for wings, female soldiers had higher FA than male soldiers but male dispersers had higher FA than female dispersers, and for femora, males and females did not differ in FA in either morph. Our results suggest that vestigial traits exhibit higher FA because of relaxation of selection for functionality, and that haploidy does not necessarily lead to increased FA in males of haplodiploid taxa.
Similar content being viewed by others
Article PDF
References
Balmford, A, Jones, I L, and Thomas, A L R. 1993. On avian asymmetry: evidence of natural selection for symmetrical tails and wings in birds. Proc R Soc B, 252, 245–251.
Beacham, T D, and Withler, R E. 1985. Heterozygosity and morphological variability of chum salmon (Oncorhynchus keta) in southern British Columbia. Heredity, 54, 313–322.
Beacham, T D, and Withler, R E. 1987. Developmental stability and heterozygosity in chum (Oncorhynchus keta) and pink (Oncorhyncus gorbuscha) salmon. Can J Zool, 65, 1823–1826.
Brückner, D. 1975. The influence of genetic variability on wing symmetry in honybees (Apis mellifera). Evolution, 30, 100–108.
Clarke, G M. 1993. The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation. Genetica, 89, 15–23.
Clarke, G M. 1995. The genetic basis of developmental stability. II. Asymmetry of extreme phenotypes revisited. Am Nat, 146, 708–725.
Clarke, G M, and Oldroyd, B P. 1996. The genetic basis of developmental stability in Apis mellifera. II. Relationships between character size, asymmetry and single-locus heterozygosity. Genetica, 97, 211–224.
Clarke, G M, Brand, G W, and Whitten, M J. 1986. Fluctuating asymmetry: a technique for measuring developmental stress caused by inbreeding. Aust J Biol Sci, 39, 145–153.
Clarke, G M, Oldroyd, B P, and Hunt, P. 1992. The genetic basis of developmental instability in Apis mellifera: heterozygosity vs. genetic balance. Evolution, 46, 753–762.
Crespi, B J. 1992a. The behavioral ecology of Australian gall thrips. J Nat Hist, 26, 769–809.
Crespi, B J. 1992b. Eusociality in Australian gall thrips. Nature, 359, 724–726.
Crespi, B J. 1993. Sex ratio selection in Thysanoptera. In: Wrensch, D. L. and Ebbert, M. (eds) Evolution and Diversity of Sex Ratio in Insects and Mites, pp. 214–234. Chapman&Hall, New York.
Crespi, B J, and Mound, L A. 1997. Ecology and evolution of social behavior among Australian gall thrips and their allies. In: Choe, J. and Crespi, B. J. (eds) The Evolution of Social Behavior in Insects and Arachnids, pp. 166–180. Cambridge University Press, Cambridge.
Crespi, B J, Carmean, D, and Chapman, T W. 1997. The ecology and evolution of galling thrips and their allies. Annu Rev Ent, 42, 51–71.
Dufour, K W, and Weatherhead, P J. 1996. Estimation of organism-wide asymmetry in red-winged blackbirds and its relation to studies of mate selection. Proc R Soc,B, 263, 769–775.
Evans, M R, and Barnard, P. 1995. Variable sexual ornaments in scarlet-tufted malachite sunbirds (Nectarinia johnstoni) on Mount Kenya. Biol J Linn Soc, 54, 371–381.
Evans, M R, Martins, T L, and Haley, M P. 1995. Inter- and intra-sexual patterns of fluctuating asymmetry in the red-billed streamertail: should symmetry always increase with ornament size? Behav Ecol Sociobiol, 37, 15–23.
Fong, D W, Kane, T C, and Culver, D C. 1995. Vestigialization and loss of non-functional characters. Ann Rev Ecol Syst, 26, 249–268.
Fowler, K, and Whitlock, M C. 1994. Fluctuating asymmetry does not increase with moderate inbreeding in Drosophila melanogaster. Heredity, 73, 373–376.
Gummer, D L, and Brigham, R M. 1995. Does fluctuating asymmetry reflect the importance of traits in little brown bats (Myotis lucifugus)? Can J Zool, 73, 990–992.
Harvey, I F, and Walsh, K J. 1993. Fluctuating asymmetry and lifetime mating success are correlated in males of the damselfly Coenagrion puella (Odonata: Coenagrionidae). Ecol Entomol, 18, 198–202.
Johnstone, R A. 1994. Female preference for symmetrical males as a by-product of selection for mate recognition. Nature, 373, 172–175.
Keller, L, and Passera, L. 1993. Incest avoidance, fluctuating asymmetry, and the consequences of inbreeding in Iridomyrmex humilis, an ant with multiple queen colonies. Behav Ecol Sociobiol, 33, 191–199.
Leary, R F, Allendorf, F W, and Knudsen, K L. 1984. Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. Am Nat, 124, 540–551.
Leary, R L, Allendorf, F W, Knudsen, K L, and Thorgaard, G H. 1985. Heterozygosity and developmental stability in gynogenetic diploid and triploid rainbow trout. Heredity, 54, 219–225.
Leung, B, and Forbes, M R. 1996. Fluctuating asymmetry in relation to stress and fitness: effects of trait type as revealed by meta-analysis. Ecoscience, 3, 400–413.
Markow, T, and Ricker, J P. 1992. Male size, developmental stability, and mating success in natural populations of three Drosophila species. Heredity, 69, 122–127.
Messier, S, and Mitton, J B. 1996. Heterozygosity at the malate dehydrogenase locus and developmental homeostasis in Apis mellifera. Heredity, 76, 616–622.
Mitton, J B. 1994. Enzyme heterozygosity, metabolism, and developmental stability. In: Markow, T. A. (ed.) Developmental Instability: its Origins and Evolutionary Implications, pp. 49–67. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Møller, A P. 1994. Sexual selection in the barn swallow (Hirundo rustica). IV. Patterns of fluctuating asymmetry and selection against asymmetry. Evolution, 48, 658–670.
Møller, A P, and Höglund, J. 1991. Patterns of fluctuating asymmetry in avian feather ornaments: implications for models of sexual selection. Proc R Soc B, 245, 1–5.
Oakes, E J, and Barnard, P. 1994. Fluctuating asymmetry and mate choice in paradise whydahs, Vidua paradisaea: an experimental manipulation. Anim Behav, 48, 937–943.
Palmer, A R. 1994. Fluctuating asymmetry analyses: a primer. In: Markow, T. A. (ed.) Developmental Instability: its Origins and Evolutionary Implications, pp. 335–364. Kluwer Academic Publishers, Dordrecht, The Netherlands.
Palmer, A R. 1996. Waltzing with asymmetry. Bioscience, 46, 518–532.
Palmer, A R, and Strobeck, C. 1986. Fluctuating asymmetry: measurement, analysis, patterns. Ann Rev Ecol Syst, 17, 391–421.
Parsons, P A. 1990. Fluctuating asymmetry: an epigenetic measure of stress. Biol Rev, 65, 131–145.
Parsons, P A. 1992. Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity, 68, 361–364.
Patterson, B D, and Patton, J L. 1990. Fluctuating asymmetry and allozymic heterozygosity among natural populations of pocket gophers (Thomomys bottae). Biol J Linn Soc, 40, 21–36.
Polak, M, and Trivers, R. 1994. The science of symmetry in biology. Trends Ecol Evol, 9, 122–124.
Roff, D A. 1990. The evolution of flightlessness in insects. Ecol Monogr, 60, 389–421.
Smith, D R, Crespi, B J, and Bookstein, F L. 1997. Asymmetry and morphological abnormality in bees Apis mellifera: effects of ploidy and hybridization J Evol Biol, (in press).
Stannard, L J. 1968. The thrips, or Thysanoptera of Illinois. Illinois Natural History Survey Bulletin, 29, 1–552.
Swaddle, J P, and Cuthill, I C. 1994. Female zebra finches prefer males with symmetric chest plumage Proc R Soc B, 258, 267–271.
Swaddle, J P, Witter, M S, and Cuthill, I C. 1994. The analysis of fluctuating asymmetry. Anim Behav, 48, 986–989.
Tague, R G. 1997. Variability of a vestigial structure: first metacarpal in Colobus guereza and Ateles geoffroyi. Evolution, 51, 595–605.
Tomkins, J L, and Simmons, L W. 1995. Patterns of fluctuating asymmetry in earwig forceps: no evidence for reliable signalling. Proc R Soc B, 259, 89–96.
Wrensch, D L, and Ebbert, M A. 1993. Evolution and Diversity of Sex Ratio in Insects and Mites Chapman&Hall, New York.
Yezerinac, S M, Lougheed, S C, and Handford, P. 1992. Measurement error and morphometric studies: statistical power and observer experience. Syst Biol, 41, 471–482.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Crespi, B., Vanderkist, B. Fluctuating asymmetry in vestigial and functional traits of a haplodiploid insect. Heredity 79, 624–630 (1997). https://doi.org/10.1038/hdy.1997.208
Received:
Issue Date:
DOI: https://doi.org/10.1038/hdy.1997.208
Keywords
This article is cited by
-
Wings are not perfect: increased wing asymmetry in a tropical butterfly as a response to forest fragmentation
The Science of Nature (2023)
-
Is Homosexuality more Prevalent in Agropastoral than in Hunting and Gathering Societies? Evidence from the Standard Cross-Cultural Sample
Adaptive Human Behavior and Physiology (2017)
-
Female Choice and the Evolution of Penis Size
Archives of Sexual Behavior (2015)
-
Flight muscle breakdown in the soldier caste of the gall-inducing thrips species, Kladothrips intermedius Bagnall
Insectes Sociaux (2014)
-
Reproductive Caste Beats a Hasty Retreat
Journal of Insect Behavior (2011)