Sexual dimorphism dominates divergent host plant use in stick insect trophic morphology

BMC Evolutionary Biology

Patrik Nosil²  Ole Seehausen³  Denis Roy¹ 

[1] EAWAG, Swiss Federal Institute of Aquatic Science & Technology, Department of Fish Ecology & Evolution, Centre for Ecology, Evolution & Biogeochemistry, Seestrasse 79, CH-6047, Kastanienbaum, Switzerland;Institute for Advanced Study, Wissenschaftskolleg, Berlin, Germany;Division of Aquatic Ecology & Evolution, Institute of Ecology & Evolution, University of Bern, Baltzerstrasse 6, CH-3012, Bern, Switzerland

关键词: Selection dissipation;    Disruptive selection;    Occupied morphospace;    Morphological uniqueness;    Bayesian clustering;    Geometric morphometrics;    Mandibles;    Trophic morphology;    Timema cristinae;    Sexual dimorphism;   

Others  :  1086971
DOI  :  10.1186/1471-2148-13-135

 received in 2013-02-08, accepted in 2013-06-18,  发布年份 2013

【 摘 要 】

Background

Clear examples of ecological speciation exist, often involving divergence in trophic morphology. However, substantial variation also exists in how far the ecological speciation process proceeds, potentially linked to the number of ecological axes, traits, or genes subject to divergent selection. In addition, recent studies highlight how differentiation might occur between the sexes, rather than between populations. We examine variation in trophic morphology in two host-plant ecotypes of walking-stick insects (Timema cristinae), known to have diverged in morphological traits related to crypsis and predator avoidance, and to have reached an intermediate point in the ecological speciation process. Here we test how host plant use, sex, and rearing environment affect variation in trophic morphology in this species using traditional multivariate, novel kernel density based and Bayesian morphometric analyses.

Results

Contrary to expectations, we find limited host-associated divergence in mandible shape. Instead, the main predictor of shape variation is sex, with secondary roles of population of origin and rearing environment.

Conclusion

Our results show that trophic morphology does not strongly contribute to host-adapted ecotype divergence in T. cristinae and that traits can respond to complex selection regimes by diverging along different intraspecific lines, thereby impeding progress toward speciation.

【 授权许可】

   
2013 Roy et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Barluenga M, Stolting KN, Salzburger W, Muschick M, Meyer A: Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 2006, 439(7077):719-723.
• [2]Grant PR, Grant BR: Evolution of Character Displacement in Darwin’s Finches. Science 2006, 313(5784):224-226.
• [3]Seehausen O, Terai Y, Magalhaes IS, Carleton KL, Mrosso HDJ, Miyagi R, Van Der Sluijs I, Schneider MV, Maan ME, Tachida H, Imai H, Okada N: Speciation through sensory drive in cichlid fish. Nature 2008, 455(7213):620-627.
• [4]Nosil P, Sandoval CP: Ecological Niche Dimensionality and the Evolutionary Diversification of Stick Insects. PLoS One 2008, 3(4):e1907.
• [5]Nosil P, Harmon LJ, Seehausen O: Ecological explanations for (incomplete) speciation. Trends Ecol Evol 2009, 24(3):145-156.
• [6]Nosil P: Ecological Speciation. 1st edition. Oxford, UK: Oxford University Press; 2012.
• [7]Coyne JA, Orr HA: Speciation. Sunderland, MA, USA: Sinauer Associates; 2004.
• [8]Gavrilets S: Fitness landscapes and the origin of speices. Princeton, NJ, USA: Princeton University Press; 2004.
• [9]Rice WR, Hostert EE: Laboratoy experiments on speciation - what have we learned in 40 years. Evolution 1993, 47(6):1637-1653.
• [10]Svanbäck R, Pineda-Krch M, Doebeli M: Fluctuating population dynamics promotes the evolution of phenotypic plasticity. Am Nat 2009, 174(2):176-189.
• [11]Rueffler C, Van Dooren TJM, Leimar O, Abrams PA: Disruptive selection and then what? Trends Ecol Evol 2006, 21(5):238-245.
• [12]Bolnick DI, Doebeli M: Sexual dimorphism and adaptive speciation: two sides of the same ecological coin. Evolution 2003, 57(11):2433-2449.
• [13]Schluter D: Ecological causes of adaptive radiation. Am Nat 1996, 148:S40-S64.
• [14]Smith TB, Skulason S: Evolutionary significance of resource polymorphisms in fishes, amphibians, and birds. Ann Rev Ecol Syst 1996, 27:111-133.
• [15]Schluter D: The Ecology of Adaptive Radiation. Oxford, UK: Oxford University Press; 2000.
• [16]Clissold FJ: The biomechanics of chewing and plant fracture: Mechanisms and implications. Adv Insect Physiol 2007, 34:317-372.
• [17]Koepfli K-P, Deere K, Slater G, Begg C, Begg K, Grassman L, Lucherini M, Veron G, Wayne R: Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation. BMC Biol 2008., 6(10)
• [18]Herrel A, Podos J, Vanhooydonck B, Hendry AP: Force-velocity trade-off in Darwin’s finch jaw function: a biomechanical basis for ecological speciation? Funct Ecol 2009, 23(1):119-125.
• [19]Lande R: Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 1980, 34(2):292-305.
• [20]Slatkin M: Ecological Causes of Sexual Dimorphism. Evolution 1984, 38(3):622-630.
• [21]Cooper IA, Gilman RT, Boughman JW: Sexual dimorphsim and speciation on two ecological coins: Patterns from nature and theoretical predictions. Evolution 2011, 65(9):2553-2571.
• [22]Ingram T, Hudson AG, Vonlanthen P, Seehausen O: Does water depth or diet divergence predict progress towards ecological speciation in whitefish radiations? Evol Ecol Res 2012, 14(4):487-502.
• [23]Clissold FJ, Sanson GD, Read J: Simpson SJ: Gross vs. net income: How plant toughness affects performance of an insect herbivore. Ecology 2009, 90(12):3393-3405.
• [24]Sandoval CP: Differential visual predation on morphs of Timema-cristinae (Phasmatodea: Timemidae) and its consequences for host-range. Biol J Linn Soc 1994, 52(4):341-356.
• [25]Nosil P, Crespi BJ: Does gene flow constrain adaptive divergence or vice versa? A test using ecomorphology and sexual isolation in Timema cristinae walking-sticks. Evolution 2004, 58(1):102-112.
• [26]Nosil P, Crespi BJ: Experimental evidence that predation promotes divergence in adaptive radiation. Proc Natl Acad Sci USA 2006, 103(24):9090-9095.
• [27]Nosil P, Crespi B, Sandoval C: Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 2002, 417(6887):440-443.
• [28]Nosil P, Crespi BJ, Sandoval CP: Reproductive isolation driven by the combined effects of ecological adaptation and reinforcement. Proc R Soc B-Biol Sci 2003, 270(1527):1911-1918.
• [29]Nosil P: Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. Am Nat 2007, 169(2):151-162.
• [30]Vickery VR: Revision of Timema Scudder (Phasmatoptera: Timematodea) including 3 new species. Can Entomol 1993, 125(4):657-692.
• [31]Crespi BJ, Sandoval CP: Phylogenetic evidence for the evolution of ecological specialization in Timema walking-sticks. J Evol Biol 2000, 13(2):249-262.
• [32]Sandoval CP, Nosil P: Counteracting selective regimes and host preference evolution in ecotypes of two species of walking-sticks. Evolution 2005, 59(11):2405-2413.
• [33]Nosil P, Crespi B, Gries R, Gries G: Natural selection and divergence in mate preference during speciation. Genetica 2007, 129(3):309-327.
• [34]Nosil P: Adaptive population divergence in cryptic color-pattern following a reduction in gene flow. Evolution 2009, 63(7):1902-1912.
• [35]Wagner KR, Ewers FW, Davis SD: Tradeoffs between hydraulic efficiency and mechanical strength in the stems of four co-occurring species of chaparral shrubs. Oecologia 1998, 117(1–2):53-62.
• [36]Patterson BD: Correlation between mandibular morphology and specific diet of some desert grassland acrididae (orthoptera). Am Mid Nat 1984, 111(2):296-303.
• [37]Bernays EA: Evolution of insect morphology in relation to plants. Philos Trans R Soc B-Biol Sci 1991, 333(1267):257-264.
• [38]Nosil P, Crespi BJ, Sandoval CP: The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks. J Evol Biol 2006, 19(3):929-942.
• [39]Tilgner EH, Kiselyova TG, McHugh JV: A morphological study of Timema cristinae vickery with implications for the phylogenetics of Phasmida. Dtsch Entomol Z 1999, 46(2):149-162.
• [40]Klingenberg CP: MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Res 2011, 11(2):353-357.
• [41]Zelditch ML, Swiderski DL, Sheets HD, Fink WL: Geometric Morphometrics for Biologists: A Primer. Amsterdam. The Netherlands: Elsevier, Academic Press; 2004.
• [42]Bookstein FL: Principal warps - thin-plate splines and the decomposition of deformations. IEEE Trans Pattern Anal Mach Intell 1989, 11(6):567-585.
• [43]Klingenberg CP: Multivariate allometry. In Advances in Morphometrics. Edited by Marcus L, Corti M, Loy A, Naylor G, DE S. New York: Plenum Press; 1996:581.
• [44]Drake AG, Klingenberg CP: The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc B-Biol Sci 2008, 275:71-76.
• [45]Hendry AP, Taylor EB, McPhail JD: Adaptive divergence and the balance between selection and gene flow: Lake and stream stickleback in the Misty system. Evolution 2002, 56(6):1199-1216.
• [46]Cheesman P, Stutz J: Bayesian classification (Autoclass): Theory and results. In Advances in Knowledge Discovery and Data Mining. Edited by Fayyad U, Ai E. Boston: MIT Press; 1996:153-188.
• [47]Rosenberg NA: DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 2004, 4(1):137-138.
• [48]Norman GR, Streiner DL: Biostatistics: The Bare Essentials . 2nd edition. Hamilton, ON Canada: B.C. Decker Inc; 2000.
• [49]Mouillot D, Stubbs W, Faure M, Dumay O, Tomasini JA, Wilson JB, Chi TD: Niche overlap estimates based on quantitative functional traits: a new family of non-parametric indices. Oecologia 2005, 145(3):345-353.
• [50]Stewart J: Single Variable Calculus: Early Trancendentals. 7th edition. Pacific Grove, CA USA: Brooks/Cole Publishing Company; 2011.
• [51]R Developement Core Team: R: A language and environment for statistical computing. In Version 2.15.1. Vienna, Austria: R Foundation for Statistical Computing; 2012. available from http://www.R-project.org webcite; accessed December 2012
• [52]Roy D, Paterson G, Hamilton PB, Heath DD, Haffner GD: Resource-based adaptive divergence in the freshwater fish Telmatherina from Lake Matano Indonesia. Mol Ecol 2007, 16(1):35-48.
• [53]Roy D, Lucek K, Bühler E, Seehausen O: Correlating shape variation with feeding performance to test for adaptive divergence in recently invading stickleback populations from Swiss peri-alpine environments. In Morphometrics for Nonmorphometricians. Edited by Elewa AMT. New York: Springer: vol. Lecture Notes in Earth Sciences 124; 2010. vol. Lecture Notes in Earth Sciences 124
• [54]Langerhans RB, DeWitt TJ: Shared and unique features of evolutionary diversification. Am Nat 2004, 164(3):335-349.
• [55]Young KA, Snoeks J, Seehausen O: Morphological diversity and the roles of contingency, chance and determinism in african cichlid radiations. PLoS One 2009, 4(3):e4740.
• [56]Sandoval CP: The effects of the relative geographic scales of gene flow and selection on morph frequencies in the walking-stick Timema cristinae. Evolution 1994, 48(6):1866-1879.
• [57]Nosil P, Crespi B, Sandoval C, Kirkpatrick M: Migration and the genetic covariance between habitat preference and performance. Am Nat 2006, 167(3):E66-E78.
• [58]Shine R: Ecological Causes for the Evolution of Sexual Dimorphism: A Review of the Evidence. Quart Rev Biol 1989, 64(4):419-461.
• [59]Andersson MB: Sexual Selection. Princeton: Oxford University Press; 1994.
• [60]Fairbairn DJ: Introduction: The enigma of sexual dimorphism. In Sex, Size & Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Edited by Fairbairn DJ, Blackenhorn WU, Székely T. Oxford, UK: Oxford University Press; 2007:266.
• [61]Nosil P, Reimchen TE: Ecological opportunity and levels of morphological variance within freshwater stickleback populations. Biol J Linn Soc 2005, 86:297-308.
• [62]Temeles EJ, Pan IL, Brennan JL, Horwitt JN: Evidence for ecological causation of sexual dimorphism in a hummingbird. Science 2000, 289(5478):441-443.
• [63]Kelly CD: Identifying a causal agent of sexual selection on weaponry in an insect. Behav Ecol 2008, 19(1):184-192.
• [64]Dijkstra PD, Seehausen O, Pierotti MER, Groothuis TGG: Male–male competition and speciation: aggression bias towards differently coloured rivals varies between stages of speciation in a Lake Victoria cichlid species complex. J Evol Biol 2007, 20(2):496-502.
• [65]Okada K, Miyanoshita A, Miyatake T: Intra-sexual Dimorphism in Male Mandibles and Male Aggressive Behavior in the Broad-Horned Flour Beetle Gnatocerus cornutus (Coleoptera: Tenebrionidae). J Insect Behav 2006, 19(4):457-467.
• [66]Gunning GE: Behavioral Observations of the Walking Stick, Anisomorpha buprestoides (Phasmatodea: Phasmatidae). Florida Ent 1987, 70(3):406-408.
• [67]Sivinski J: Iintrasexual aggression in the stick insects Diapheromera velei and D. covilleae and sexual dimorphism in the Phasmatodea. Psyche 1978, 85:395-405.
• [68]Arbuthnott D, Crespi BJ: Courtship and mate discrimination within and between species of Timema walking-sticks. Anim Behv 2009, 78(1):53-59.
• [69]Temeles EJ, Kress WJ: Adaptation in a Plant-Hummingbird Association. Science 2003, 300(5619):630-633.
• [70]Herler J, Kerschbaumer M, Mitteroecker P, Postl L, Sturmbauer C: Sexual dimorphism and population divergence in the Lake Tanganyika cichlid fish genus Tropheus. Front Zool 2010, 7(1):4. BioMed Central Full Text
• [71]Butler MA, Sawyer SA, Losos JB: Sexual dimorphism and adaptive radiation in Anolis lizards. Nature 2007, 447(May):202-205.
• [72]Pfaender J, Miesen FW, Hadiaty RK, Herder F: Adaptive speciation and sexual dimorphism contribute to diversity in form and function in the adaptive radiation of Lake Matano’s sympatric roundfin sailfin silversides. J Evol Biol 2011, 24(11):2329-2345.
• [73]Sanson G: The biomechanics of browsing and grazing. Am J Bot 2006, 93(10):1531-1545.
• [74]Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP: Stable isotopes in plant ecology. Annu Rev Ecol Evol Syst 2002, 33:507-559.
• [75]Guelke M, Von Blanckenburg F: Fractionation of Stable Iron Isotopes in Higher Plants. Environ Sci Tech 2007, 41(6):1896-1901.
• [76]Webb JA, Bond NR, Wealands SR, Mac Nally R, Quinn GP, Vesk PA, Grace MR: Bayesian clustering with AutoClass explicitly recognises uncertainties in landscape classification. Ecography 2007, 30(4):526-536.