Abstract
Much of the morphological diversity in nature—including among sexes within a species—is a direct consequence of variation in size and shape. However, disentangling variation in sexual dimorphism for both shape (SShD), size (SSD), and their relationship with one another remains complex. Understanding how genetic variation influences both size and shape together, and how this in turn influences SSD and SShD, is challenging. In this study, we utilize Drosophila wing size and shape as a model system to investigate how mutations influence size and shape as modulated by sex. Previous work has demonstrated that mutations in epidermal growth factor receptor (EGFR) and transforming growth factor-β (TGF-β) signaling components can influence both wing size and shape. In this study, we re-analyze this data to specifically address how they impact the relationship between size and shape in a sex-specific manner, in turn altering the pattern of sexual dimorphism. While most mutations influence shape overall, only a subset have a genotypic specific effect that influences SShD. Furthermore, while we observe sex-specific patterns of allometric shape variation, the effects of most mutations on allometry tend to be small. We discuss this within the context of using mutational analysis to understand sexual size and shape dimorphism.
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References
Abbott JK, Bedhomme S, Chippindale AK (2010) Sexual conflict in wing size and shape in Drosophila melanogaster. J Evol Biol 23(9):1989–1997, Available at http://www.ncbi.nlm.nih.gov/pubmed/20695965
Abu-Shaar M, Mann RS (1998) Generation of multiple antagonistic domains along the proximodistal axis during Drosophila leg development. Development 125(19):3821–3830, Available at http://www.ncbi.nlm.nih.gov/pubmed/9729490
Allen CE, Zwaan BJ, Brakefield PM (2011) Evolution of sexual dimorphism in the Lepidoptera. Annu Rev Entomol 56:445–464, Available at http://www.ncbi.nlm.nih.gov/pubmed/20822452
Bird MA, Schaffer HE (1972) A study of the genetic basis of the sexual dimorphism for wing length in Drosophila melanogaster. Genetics 72(3):475–487
Blanckenhorn WU et al (2007) Proximate causes of Rensch’s rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am Nat 169(2):245–257
Bolstad, G.H. et al., 2015. Complex constraints on allometry revealed by artificial selection on the wing of Drosophila melanogaster. Proc Natl Acad Sci U S A, 112(43), p.201505357. Available at http://www.pnas.org/lookup/doi/10.1073/pnas.1505357112
Bonduriansky R (2007) Sexual selection and allometry: a critical reappraisal of the evidence and ideas. Evolution 61(4):838–849, Available at http://www.ncbi.nlm.nih.gov/pubmed/17439616
Bonduriansky R, Chenoweth SF (2009) Intralocus sexual conflict. Trends Ecol Evol 24(5):280–288, Available at http://www.ncbi.nlm.nih.gov/pubmed/19307043
Bonduriansky R, Day T (2003) The evolution of static allometry in sexually selected traits. Evolution 57(11):2450–2458, Available at http://www.ncbi.nlm.nih.gov/pubmed/14686522
Carreira VP et al (2011) Genetic basis of wing morphogenesis in Drosophila: sexual dimorphism and non-allometric effects of shape variation. BMC Dev Biol 11(1):32, Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3129315&tool=pmcentrez&rendertype=abstract
Chandler CH, Chari S, Dworkin I (2013) Does your gene need a background check? How genetic background impacts the analysis of mutations, genes, and evolution. Trends Genet 29(6):358–366, Available at http://linkinghub.elsevier.com/retrieve/pii/S0168952513000218
Collyer ML, Sekora DJ, Adams DC (2015) A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115(4):357–365, Available at http://www.nature.com/doifinder/10.1038/hdy.2014.75
Cox RM, Calsbeek R (2010) Sex-specific selection and intraspecific variation in sexual size dimorphism. Evolution 64(3):798–809, Available at http://www.ncbi.nlm.nih.gov/pubmed/19796147
David JR et al (2003) Genetic variability of sexual size dimorphism in a natural population of Drosophila melanogaster: an isofemale-line approach. J Genet 82(3):79–88, Available at http://www.ncbi.nlm.nih.gov/pubmed/15133187
Day SJ, Lawrence PA (2000) Measuring dimensions: the regulation of size and shape. Development 127(14):2977–2987, Available at http://www.ncbi.nlm.nih.gov/pubmed/10862736
de Moed GH, De Jong G, Scharloo W (1997) Environmental effects on body size variation in Drosophila melanogaster and its cellular basis. Genet Res 70(1):35–43, Available at http://www.ncbi.nlm.nih.gov/pubmed/9369097
Drake AG, Klingenberg CP (2008) The pace of morphological change: historical transformation of skull shape in St. Bernard dogs. Proc R Soc B Biol Sci 275(1630):71–76
Dworkin I, Gibson G (2006) Epidermal growth factor receptor and transforming growth factor-beta signaling contributes to variation for wing shape in Drosophila melanogaster. Genetics 173(3):1417–1431
Emlen DJ (1996) Artificial selection on horn length-body size allometry in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Evolution 50(3):1219–1230
Fairbairn DJ (1990) Factors influencing sexual size dimorphism in temperate waterstriders. Am Nat 136(1):61–86
Fairbairn DJ (2005) Allometry for sexual size dimorphism: testing two hypotheses for Rensch’s rule in the water strider Aquarius remigis. Am Nat 166(4):69–84, Available at http://www.ncbi.nlm.nih.gov/pubmed/16224713
Fairbairn DJ, Blanckenhorn WU (2007) Sex, size, and gender roles: evolutionary studies of sexual size dimorphism. Oxford University Press, Oxford
Fairbairn DJ, Roff DA (2006) The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage. Heredity 97(5):319–328
Ferguson IM, Fairbairn DJ (2000) Sex-specific selection and sexual size dimorphism in the waterstrider Aquarius remigis. J Evol Biol 13(2):160–170
Frankino WA et al (2005) Natural selection and developmental constraints in the evolution of allometries. Science (New York, NY) 307(5710):718–720, Available at http://www.ncbi.nlm.nih.gov/pubmed/15692049
Gao X, Pan D (2001) TSC1 and TSC2 tumor suppressors antagonize insulin signaling in cell growth. Genes Dev 15(11):1383–1392, Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=312704&tool=pmcentrez&rendertype=abstract
García-Bellido A, Cortés F, Milán M (1994) Cell interactions in the control of size in Drosophila wings. Proc Natl Acad Sci U S A 91(21):10222–10226, Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=44990&tool=pmcentrez&rendertype=abstract
Ghosh SM, Testa ND, Shingleton AW (2013) Temperature-size rule is mediated by thermal plasticity of critical size in Drosophila melanogaster. Proc R Soc B Biol Sci 280(1760):20130174–20130174, Available at http://rspb.royalsocietypublishing.org/cgi/doi/10.1098/rspb.2013.0174
Gidaszewski NA, Baylac M, Klingenberg C (2009) Evolution of sexual dimorphism of wing shape in the Drosophila melanogaster subgroup. BMC Evol Biol 9(1):110, Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2691407&tool=pmcentrez&rendertype=abstract
Gould SJ (1966) Allometry and size in ontogeny and phylogeny. Biol Rev Camb Philos Soc 41(4):587–640, Available at http://www.ncbi.nlm.nih.gov/pubmed/5342162
Hedrick AV, Temeles EJ (1989) The evolution of sexual dimorphism in animals: hypotheses and tests. Trends Ecol Evol 4(5):136–138
Horabin JI (2005) Splitting the hedgehog signal: sex and patterning in Drosophila. Development 132(21):4801–4810
Huxley J (1932) Problems of relative growth. Lincoln MacVeagh, The Dial Press, New York
Kijimoto T, Moczek AP, Andrews J (2012) Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns. Proc Natl Acad Sci U S A 109(50):20526–20531, Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3528601&tool=pmcentrez&rendertype=abstract
Kirkwood TBL et al (2005) What accounts for the wide variation in life span of genetically identical organisms reared in a constant environment? Mech Ageing Dev 126(3):439–443, Available at http://www.ncbi.nlm.nih.gov/pubmed/15664632
Lavine L, Gotoh H, Brent CS, Dworkin I, Emlen DJ (2015) Exaggerated trait growth in insects. Annu Rev Entomol 60:453–472
Lovich JE, Gibbons JW (1992) A review of techniques quantifying sexual size dimorphism. Growth Dev Aging 56:269–281
Mank JE (2009) Sex chromosomes and the evolution of sexual dimorphism: lessons from the genome. Am Nat 173(2):141–150
Merila AJ et al (2011) Quantitative genetics of sexual size dimorphism in the collared flycatcher, Ficedula albicollis. Society 52(3):870–876
Mosimann JE (1970) Size allometry: size and shape variables with characterizations of the lognormal and generalized gamma distributions. J Am Stat Assoc 65(330):930–945
Nevill AM, Holder RL, Alan M (1995) Scaling, normalizing and per ratio an allometric modeling approach standards: an allometric modeling approach. J Appl Physiol 79(3):1027–1931
Paaby AB, Rockman MV (2014) Cryptic genetic variation: evolution’s hidden substrate. Nat Rev Genet 15(4):247–258, Available at http://www.nature.com/doifinder/10.1038/nrg3688
Palsson A, Gibson G (2004) Association between nucleotide variation in EGFR and wing shape in Drosophila melanogaster. Genetics 167(3):1187–1198
Prasad NG et al (2007) An evolutionary cost of separate genders revealed by male-limited evolution. Am Nat 169(1):29–37, Available at http://www.ncbi.nlm.nih.gov/pubmed/17206582
Preziosi RF, Fairbairn DJ (2000) Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism. Evolution 54(2):558–566
Prober DA, Edgar BA (2000) Ras1 promotes cellular growth in the Drosophila wing. Cell 100(4):435–446
Raj A, van Oudenaarden A (2008) Nature, nurture, or chance: stochastic gene expression and its consequences. Cell 135(2):216–226, Available at http://www.ncbi.nlm.nih.gov/pubmed/18957198
Rea SL et al (2005) A stress-sensitive reporter predicts longevity in isogenic populations of Caenorhabditis elegans. Nat Genet 37(8):894–898
Reeve JP, Fairbairn DJ (1996) Sexual size dimorphism as a correlated response to selection on body size: an empirical test of the quantitative genetic model. Evolution 50(5):1927–1938
Reeve JP, Fairbairn DJ (1999) Change in sexual size dimorphism as a correlated response to selection on fecundity. Heredity 83(6):697–706, Available at http://www.ncbi.nlm.nih.gov/pubmed/10651914
Reeve JP, Fairbairn DJ (2001) Predicting the evolution of sexual size dimorphism. J Evol Biol 14(2):244–254, Available at http://doi.wiley.com/10.1046/j.1420-9101.2001.00276.x
Rideout EJ, Marshall L, Grewal SS (2012) Drosophila RNA polymerase III repressor Maf1 controls body size and developmental timing by modulating tRNAiMet synthesis and systemic insulin signaling. Proc Natl Acad Sci U S A 109(4):1139–1144
Rohlf, F.J., 2003. TpsDig. http://life.bio.sunysb.edu/morph/
Sanger TJ et al (2013) Convergent evolution of sexual dimorphism in skull shape using distinct developmental strategies. Evolution 67(8):2180–2193, Available at http://doi.wiley.com/10.1111/evo.12100
Shine R (1989) Ecological causes for the evolution of sexual dimorphism: a review of the evidence. Q Rev Biol 64(4):419–461, Available at http://www.jstor.org/stable/2830103
Shingleton AW et al (2005) The temporal requirements for insulin signaling during development in Drosophila. PLoS Biol 3(9), e289
Shingleton AW et al (2009) Many ways to be small: different environmental regulators of size generate distinct scaling relationships in Drosophila melanogaster. Proc R Soc B Biol Sci 276(1667):2625–2633, Available at http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2686648&tool=pmcentrez&rendertype=abstract
Smith RJ (1999) Statistics of sexual size dimorphism. J Hum Evol 36(4):423–458, Available at http://linkinghub.elsevier.com/retrieve/pii/S0047248498902810
Stern DL, Emlen DJ (1999) The developmental basis for allometry in insects. Development 126(6):1091–1101, Available at http://www.ncbi.nlm.nih.gov/pubmed/10021329
Takahashi KH, Blanckenhorn WU (2015) Effect of genomic deficiencies on sexual size dimorphism through modification of developmental time in Drosophila melanogaster. Heredity 115(2):140–145, Available at http://www.nature.com/doifinder/10.1038/hdy.2015.1
Tatar M et al (2001) A mutant Drosophila insulin receptor homolog that extends life-span and impairs neuroendocrine function. Science (New York, NY) 292(5514):107–110, Available at http://www.ncbi.nlm.nih.gov/pubmed/11292875
Testa, N.D., Ghosh, S.M. & Shingleton, A.W., 2013. Sex-specific weight loss mediates sexual size dimorphism in Drosophila melanogaster. F. Pichaud, ed. PLoS ONE, 8(3), p.e58936. Available at http://dx.plos.org/10.1371/journal.pone.0058936.
Thompson DW (1917) On growth and form. Cambridge University Press, Cambridge
van der Linde K, Houle D (2009) Inferring the nature of allometry from geometric data. Evol Biol 36(3):311–322, Available at http://link.springer.com/10.1007/s11692-009-9061-z
Weatherbee SD et al (1998) Ultrabithorax regulates genes at several levels of the wing-patterning hierarchy to shape the development of the Drosophila haltere. Genes Dev 12(10):1474–1482, Available at http://www.genesdev.org/cgi/doi/10.1101/gad.12.10.1474
Weber K (2005) Many P-element insertions affect wing shape in Drosophila melanogaster. Genetics 169(3):1461–1475, Available at http://www.genetics.org/cgi/doi/10.1534/genetics.104.027748
Weinkove D et al (1999) Regulation of imaginal disc cell size, cell number and organ size by Drosophila class I(A) phosphoinositide 3-kinase and its adaptor. Curr Biol 9(18):1019–1029, Available at http://www.ncbi.nlm.nih.gov/pubmed/10508611
Acknowledgments
We would like to thank Dr. William Pitchers for providing us with R scripts that facilitated the analysis.
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This work was supported by NIH grant 1R01GM094424–01 and an NSERC Discovery award to ID.
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The authors declare that they have no conflict of interest.
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Communicated by Nico Posnien and Nikola-Michael Prpic
Data archiving: http://dx.doi.org/10.5061/dryad.1041
Scripts will be archived on https://github.com/DworkinLab/TestaDworkin2016DGE
This article is part of the Special issue “Size and shape: integration of morphometrics, mathematical modeling, developmental and evolutionary biology”, Guest Editors: Nico Posnien—Nikola-Michael Prpic.
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Supplementary Fig. 1
Magnitude of SSD and SShD for 42 mutants in Oregon-R (left) and Samarkand (right) wild type backgrounds, after correcting for the influence of allometry (shape on size). A common allometry relationship was assumed across genotype and sex within each background and line combination. Residuals from the allometric model were then used for the analysis. This figure is otherwise identical to figure 2 (which does not correct for allometry). The effect of each mutant is mapped out in a size-and-shape dimorphism space. Genotypic means for each mutant are indicated by point style and connected by a solid line. SSD is plotted on each x-axis for all plots and SShD is displayed on the y-axis. The plots above display the entire range of variation observed, while those below display only the area with the highest density of points. Lines with significant sex-by-genotype effects are highlighted as follows: effect on both size and shape, shape only and size only. Only significant genes (after sequential Bonferroni correction) from the linear models are colored. Error bars are 95% confidence intervals (unadjusted alpha). All gene names are displayed lowercase, regardless of dominance (GIF 62 kb)
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Testa, N.D., Dworkin, I. The sex-limited effects of mutations in the EGFR and TGF-β signaling pathways on shape and size sexual dimorphism and allometry in the Drosophila wing. Dev Genes Evol 226, 159–171 (2016). https://doi.org/10.1007/s00427-016-0534-7
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DOI: https://doi.org/10.1007/s00427-016-0534-7