Evolution of Morphological Integration: Developmental Accommodation of Stress‐Induced Variation

Extreme environmental change during growth often results in an increase in developmental abnormalities in the morphology of an organism. The evolutionary significance of such stress‐induced variation depends on the recurrence of a stressor and on the degree to which developmental errors can be accommodated by an organism’s ontogeny without significant loss of function. We subjected populations of four species of soricid shrews to an extreme environment during growth and measured changes in the patterns of integration and accommodation of stress‐induced developmental errors in a complex of mandibular traits. Adults that grew under an extreme environment had lower integration of morphological variation among mandibular traits and highly elevated fluctuating asymmetry in these traits, compared to individuals that grew under the control conditions. However, traits differed strongly in the magnitude of response to a stressor—traits within attachments of the same muscle (functionally integrated traits) had lower response and changed their integration less than other traits. Cohesiveness in functionally integrated complexes of traits under stress was maintained by close covariation of their developmental variation. Such developmental accommodation of stress‐induced variation might enable the individual’s functioning and persistence under extreme environmental conditions and thus provides a link between individual adaptation to stress and the evolution of stress resistance.

[1]  S. Herring,et al.  Jaw muscles and the skull in mammals: the biomechanics of mastication. , 2000, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[2]  M. Moss,et al.  The primary role of functional matrices in facial growth. , 1969, American journal of orthodontics.

[3]  R. K. Rose,et al.  Advances in the biology of shrews , 1994 .

[4]  A. Badyaev,et al.  Extreme environmental change and evolution: stress-induced morphological variation is strongly concordant with patterns of evolutionary divergence in shrew mandibles , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  Stuart A. Newman,et al.  24 – Epigenetic Mechanisms of Character Origination , 2001 .

[6]  A. Badyaev Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation , 2005, Proceedings of the Royal Society B: Biological Sciences.

[7]  W. Atchley,et al.  QUANTITATIVE GENETICS OF DEVELOPMENT: GENETIC CORRELATIONS AMONG AGE‐SPECIFIC TRAIT VALUES AND THE EVOLUTION OF ONTOGENY , 1983, Evolution; international journal of organic evolution.

[8]  A. Isberg,et al.  Mandibular length and midline asymmetry after experimentally induced temporomandibular joint disk displacement in rabbits. , 1999, American journal of orthodontics and dentofacial orthopedics : official publication of the American Association of Orthodontists, its constituent societies, and the American Board of Orthodontics.

[9]  Günter P. Wagner,et al.  Complex Adaptations and the Evolution of Evolvability , 2005 .

[10]  L. Leamy,et al.  Morphological integration of fluctuating asymmetry in the mouse mandible , 1993, Genetica.

[11]  B. Riska COMPOSITE TRAITS, SELECTION RESPONSE, AND EVOLUTION , 1989, Evolution; international journal of organic evolution.

[12]  G B Müller,et al.  Epigenetic mechanisms of character origination. , 2000, The Journal of experimental zoology.

[13]  A. Hoffmann,et al.  Environmental Stress as an Evolutionary Force , 2000 .

[14]  Greg Gibson,et al.  Uncovering cryptic genetic variation , 2004, Nature Reviews Genetics.

[15]  Ch. Dötsch Mastication in the musk shrew, Suncus murinus (mammalia, Soricidae) , 1986, Journal of morphology.

[16]  M. West-Eberhard Developmental plasticity and evolution , 2003 .

[17]  Morphological integration of fluctuating asymmetry in the mouse mandible , 1993 .

[18]  A. Imasheva [Environmental stress and genetic variation in animal populations]. , 1999, Genetika.

[19]  B. Hallgrímsson Ontogenetic Patterning of Skeletal Fluctuating Asymmetry in Rhesus Macaques and Humans: Evolutionary and Developmental Implications , 1999, International Journal of Primatology.

[20]  Christian Peter Klingenberg,et al.  GEOMETRIC MORPHOMETRICS OF DEVELOPMENTAL INSTABILITY: ANALYZING PATTERNS OF FLUCTUATING ASYMMETRY WITH PROCRUSTES METHODS , 1998, Evolution; international journal of organic evolution.

[21]  F. Stuart Chapin,et al.  Evolution of Suites of Traits in Response to Environmental Stress , 1993, The American Naturalist.

[22]  D. Roff Phenotypic Evolution — A Reaction Norm Perspective , 1999, Heredity.

[23]  J. Juste,et al.  Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalia: Megachiroptera) from the islands of the Gulf of Guinea. II. Integration and levels of multivariate fluctuating asymmetry across a geographical range , 2001 .

[24]  C. Klingenberg,et al.  Inferring Developmental Modularity from Morphological Integration: Analysis of Individual Variation and Asymmetry in Bumblebee Wings , 2001, The American Naturalist.

[25]  Augusta Ärnbäck-Christie-Linde Der Bau der Soriciden und ihre Beziehungen zu andern Säugetieren , 1907 .

[26]  A. Badyaev,et al.  Evolution of Morphological Integration. I. Functional Units Channel Stress‐Induced Variation in Shrew Mandibles , 2004, The American Naturalist.

[27]  Katherine E. Willmore,et al.  Craniofacial variability and modularity in macaques and mice. , 2004, Journal of Experimental Zoology Part B: Molecular and Developmental Evolution.

[28]  C. Strobeck,et al.  Fluctuating Asymmetry Analyses Revisited , 2001 .

[29]  G. Wagner,et al.  Adaptive Inertia Caused by Hidden Pleiotropic Effects , 1997 .

[30]  A. Badyaev,et al.  STRESS AND DEVELOPMENTAL STABILITY: VEGETATION REMOVAL CAUSES INCREASED FLUCTUATING ASYMMETRY IN SHREWS , 2000 .

[31]  A. Bradshaw,et al.  Evolution and stress-genotypic and phenotypic components , 1989 .

[32]  A. Meyer Morphometrics and allometry in the trophically polymorphic cichlid fish, Cichlasoma citrinellum: Alternative adaptations and ontogenetic changes in shape , 1990 .

[33]  R. Bonal,et al.  Why do some traits show higher fluctuating asymmetry than others? A test of hypotheses with tail feathers of birds , 2002, Heredity.

[34]  P. Wimberger PLASTICITY OF JAW AND SKULL MORPHOLOGY IN THE NEOTROPICAL CICHLIDS GEOPHAGUS BRASILIENSIS AND G. STEINDACHNERI , 1991, Evolution; international journal of organic evolution.

[35]  M. Pigliucci,et al.  Phenotypic Evolution: A Reaction Norm Perspective , 1998 .

[36]  L. Ancel,et al.  A quantitative model of the Simpson-Baldwin Effect. , 1999, Journal of theoretical biology.

[37]  I. Schmalhausen,et al.  Factors of evolution , 1949 .

[38]  R. German,et al.  The epigenetic impact of weaning on craniofacial morphology during growth. , 1996, The Journal of experimental zoology.

[39]  M. West-Eberhard Phenotypic Plasticity and the Origins of Diversity , 1989 .

[40]  H. F. Nijhout,et al.  The nature of robustness in development. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[41]  S. Herring,et al.  Cranial sutures and bones: growth and fusion in relation to masticatory strain. , 2004, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[42]  C. Wills The Possibility of Stress-Triggered Evolution , 1984 .

[43]  Susan Oyama The Ontogeny of Information: Developmental Systems and Evolution , 2000 .

[44]  R. German,et al.  Ontogeny of feeding function in the gray short-tailed opossum Monodelphis domestica: empirical support for the constrained model of jaw biomechanics , 2003, Journal of Experimental Biology.

[45]  P. Calow,et al.  Environmental Stress, Adaptation and Evolution , 1997, Experientia Supplementum.

[46]  V. Debat,et al.  Mapping phenotypes: canalization, plasticity and developmental stability , 2001 .

[47]  A. R. Palmer Symmetry Breaking and the Evolution of Development , 2004, Science.

[48]  K. Foresman,et al.  The Reproductive Cycles of the Vagrant Shrew (Sorex vagrans) and the Masked Shrew (Sorex cinereus) in Montana , 1998 .

[49]  R. German,et al.  Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. , 2000, The Journal of nutrition.

[50]  B. Hall Unlocking the Black Box between Genotype and Phenotype: Cell Condensations as Morphogenetic (modular) Units , 2003 .

[51]  George V. Lauder,et al.  Form and function: structural analysis in evolutionary morphology , 1981, Paleobiology.

[52]  I. Eshel,et al.  Canalization, genetic assimilation and preadaptation. A quantitative genetic model. , 1998, Genetics.

[53]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.

[54]  L. Lens,et al.  Fluctuating and directional asymmetry in natural bird populations exposed to different levels of habitat disturbance, as revealed by mixture analysis , 2000 .

[55]  J. Swaddle,et al.  On the ontogeny of developmental stability in a stabilized trait , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  C. Waddington,et al.  GENETIC ASSIMILATION OF AN ACQUIRED CHARACTER , 1953 .

[57]  D. Wake,et al.  Trends in the functional morphology and sensorimotor control of feeding behavior in salamanders: An example of the role of internal dynamics in evolution , 1985, Acta biotheoretica.

[58]  S. Rutherford,et al.  Between genotype and phenotype: protein chaperones and evolvability , 2003, Nature Reviews Genetics.

[59]  C. Schlichting,et al.  Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes , 2002, Evolutionary Ecology.

[60]  Bruce Riska,et al.  SOME MODELS FOR DEVELOPMENT, GROWTH, AND MORPHOMETRIC CORRELATION , 1986, Evolution; international journal of organic evolution.

[61]  D. R. Sharma Studies on the anatomy of the indian insectivore, suncus murinus. , 1958 .

[62]  B. Hallgrímsson Fluctuating Asymmetry in the Mammalian Skeleton , 1988 .

[63]  F. Rohlf,et al.  Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks , 1990 .

[64]  F. Witte,et al.  DIFFERENCES BETWEEN INTER- AND INTRASPECIFIC ARCHITECTONIC ADAPTATIONS TO PHARYNGEAL MOLLUSC CRUSHING IN CICHLID FISHES , 1996 .

[65]  G. Huether The central adaptation syndrome: Psychosocial stress as a trigger for adaptive modifications of brain structure and brain function , 1996, Progress in Neurobiology.

[66]  Erry,et al.  DEVELOPMENTAL INSTABILITY AND THE ENVIRONMENT : WHY ARE SOME SPECIES OF SHREWS BETTER INDICATORS OF STRESS THAN OTHERS ? , 2006 .

[67]  Garth A. Gibson,et al.  Canalization in evolutionary genetics: a stabilizing theory? , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[68]  Colin D. Meiklejohn,et al.  A single mode of canalization , 2002 .

[69]  Hod Lipson,et al.  ON THE ORIGIN OF MODULAR VARIATION , 2002, Evolution; international journal of organic evolution.

[70]  G. Gaughran A comparative study of the osteology and myology of the cranial and cervical regions of the shrew, Blarina brevicauda, and the mole, Scalopus aquaticus. , 1954 .

[71]  D. Laskin,et al.  Preadaptive potentialities of the mammalian skull: an experiment in growth and form. , 1961, The American journal of anatomy.

[72]  J. Cheverud PHENOTYPIC, GENETIC, AND ENVIRONMENTAL MORPHOLOGICAL INTEGRATION IN THE CRANIUM , 1982, Evolution; international journal of organic evolution.

[73]  L. Hadany,et al.  On the evolutionary advantage of fitness-associated recombination. , 2003, Genetics.

[74]  C. Waddington Evolution of Developmental Systems , 1941, Nature.

[75]  J. Hanken,et al.  Jaw muscle development as evidence for embryonic repatterning in direct–developing frogs , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  L. Caporale Chance Favors the Prepared Genome , 1999, Annals of the New York Academy of Sciences.

[77]  E. Jablonka,et al.  Epigenetic Inheritance and Evolution: The Lamarckian Dimension , 1995 .

[78]  D. Hartl,et al.  GENETIC CONTROL OF THE RATE OF EMBRYONIC DEVELOPMENT: SELECTION FOR FASTER DEVELOPMENT AT ELEVATED TEMPERATURES , 1993, Evolution; international journal of organic evolution.

[79]  D. Irwin,et al.  The role of phenotypic plasticity in driving genetic evolution , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[80]  G. Wagner,et al.  A POPULATION GENETIC THEORY OF CANALIZATION , 1997, Evolution; international journal of organic evolution.

[81]  D. Waxman,et al.  Pleiotropy and the preservation of perfection. , 1998, Science.

[82]  A. Hoffmann,et al.  Extreme environmental change and evolution , 1997 .

[83]  V. Loeschcke,et al.  Environmental stress, adaptation and evolution: an overview , 2005, Journal of evolutionary biology.

[84]  A. Badyaev Environmental stress and developmental stability in dentition of the Yellowstone grizzly bears , 1998 .

[85]  Imasheva Ag Environmental stress and genetic variation in animal populations , 1999 .

[86]  S. Rice THE EVOLUTION OF CANALIZATION AND THE BREAKING OF VON BAER'S LAWS: MODELING THE EVOLUTION OF DEVELOPMENT WITH EPISTASIS , 1998, Evolution; international journal of organic evolution.

[87]  B. Hallgrímsson,et al.  Embryological origins of developmental stability: size, shape and fluctuating asymmetry in prenatal random bred mice. , 2003, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[88]  R. Goldschmidt,et al.  The material basis of evolution , 1941 .

[89]  A. Bergman,et al.  Waddington's canalization revisited: Developmental stability and evolution , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[90]  I. Hanski,et al.  Developmental Stability and Population Dynamics in the Common Shrew, Sorex araneus , 1991, The American Naturalist.

[91]  AN EXPERIMENTAL STUDY OF INTRASPECIFIC VARIATION, DEVELOPMENTAL TIMING, AND HETEROCHRONY IN FISHES , 2000, Evolution; international journal of organic evolution.

[92]  P. Alberch Ontogenesis and Morphological Diversification , 1980 .

[93]  M. Pigliucci,et al.  Phenotypic plasticity and evolution by genetic assimilation , 2006, Journal of Experimental Biology.

[94]  S. Herring,et al.  Age changes in mastication in the pig. , 1994, Comparative biochemistry and physiology. Comparative physiology.