Size variation, growth strategies, and the evolution of modularity in the mammalian skull

Evolution

Volumn 67, Issue 11, 2013, Pages 3305-3322

  Porto, Arthur ^a,b   Shirai, Leila Teruko ^c   de Oliveira, Felipe Bandoni ^b   Marroig, Gabriel ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Allometry; Constraints; Flexibility; Life history evolution; Morphospace; V CV matrix

Indexed keywords

ALLOMETRY; EVOLUTIONARY BIOLOGY; INTERSPECIFIC VARIATION; LIFE HISTORY TRAIT; MAMMAL; MORPHOLOGY; NATURAL SELECTION; SIZE; SKULL;

MAMMALIA;

ALLOMETRY; ANIMAL; ARTICLE; CONSTRAINTS; EVOLUTION; FEMALE; FLEXIBILITY; GENETIC SELECTION; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; HUMAN; LIFE-HISTORY EVOLUTION; MALE; MAMMAL; MORPHOSPACE; PHYLOGENY; REGRESSION ANALYSIS; SKULL; SPECIES DIFFERENCE; V/CV MATRIX;

ALLOMETRY; CONSTRAINTS; FLEXIBILITY; LIFE-HISTORY EVOLUTION; MORPHOSPACE; V/CV MATRIX;

ANIMALS; BIOLOGICAL EVOLUTION; FEMALE; HUMANS; MALE; MAMMALS; PHYLOGENY; REGRESSION ANALYSIS; SELECTION, GENETIC; SKULL; SPECIES SPECIFICITY;

EID: 84886247859     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/evo.12177     Document Type: Article

References (60)

1. Arnold, S. J. 1992. Constraints on phenotypic evolution. Am. Nat. 140:S85-S107.
2. Arnold, S. J., M. E. Pfrender, and A. G. Jones 2001. The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112-113:9-32.
3. Armbruster, W. S., C. Pélabon, T. F. Hansen, and C. P. H. Mulder 2004. Floral integration, modularity, and accuracy: distinguishing complex adaptations from genetic constraints. Pp. 23-49 in M. Pigliucci and K. Preston, eds. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford Univ. Press, Oxford, U.K.
4. Badyaev, A. V., and K. R. Foresman 2004. Evolution of morphological integration. I. Functional units channel stress-induced variation in shrew mandibles. Am. Nat. 163:868-879.
5. Berg, R. L. 1960. The ecological significance of correlation pleiades. Evolution 14:171-180.
6. Bininda-Emonds, O. R. P., M. Cardillo, K. E. Jones, R. D. E. MacPhee, R. M. D. Beck, R. Grenyer, S. A. Price, R. A. Vos, J. L. Gittleman, and A. Purvis 2007. The delayed rise of present-day mammals. Nature 446:507-512.
7. Chernoff, B., and P. M. Magwene 1999. Morphological integration: fourty years later. Pp. 316-360 in E. C. Olson and R. L. Miller Morphological integration. University of Chicago Press, Chicago, IL.
8. Cheverud, J. M. 1982. Phenotypic, genetic and environmental morphological integration in the cranium. Evolution 36:499-516.
9. Cheverud, J. M.. 1984. Quantitative genetics and developmental constraints on evolution by selection. J. Theor. Biol. 110:155-172.
10. Cheverud, J. M.. 1988. A comparison of genetic and phenotypic correlations. Evolution 42:958-968.
11. Cheverud, J. M.. 1995. Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. Am. Nat. 145:63-89.
12. Cheverud, J. M.. 1996. Quantitative genetic analysis of cranial morphology in the cotton-top (Saguinus oedipas) and saddle-back (S. fuscicollis) tamarins. J. Evol. Biol. 9:5-42.
13. Delph, L. F., J. C. Steven, I. A. Anderson, C. R. Herlihy, and E. D. Brodie III. 2011. Elimination of a genetic correlation between the sexes via artificial correlational selection. Evolution 65:2872-2880.
14. Eble, G. 2004. The macroevolution of phenotypic integration. Pp. 253-273 in M. Pigliucci and K. Preston, eds. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford Univ. Press, Oxford, U.K.
15. Emerson, S. B., and P. A. Hastings 1998. Morphological correlations in evolution: consequences for phylogenetic analyses. Quart. Rev. Biol. 73:141-162.
16. Hansen, T. F., and D. Houle 2008. Measuring and comparing evolvability and constraint in multivariate characters. J. Evol. Biol. 21:1201-1219.
17. Hansen, T. F., and K. L. Voje 2011. Deviation from the line of least resistance does not exclude genetic constraints: a comment on Berner et al. (2010). Evolution 65:1821-1822.
18. Harmon, L. K., and R. E. Glor 2010. Poor statistical performance of the Mantel test in comparative phylogenetic analyses. Evolution 64:2173-2178.
19. Hayssen, V., Ari van Tienhoven, and Ans van Tienhoven 1993. Asdell's patterns of mammalian reproduction: a compendium of species-specific data. Cornell Univ. Press, New York.
20. Huxley, J. S. 1932. Problems of relative growth. Johns Hopkins Univ. Press, Baltimore, MD.
21. Jacob, F. 1977. Evolution and tinkering. Science 196:1161-1166.
22. Jones, K. E., J. Bielby, M. Cardillo, S. A. Fritz, J. O'Dell, C. D. L. Orme, K. Safi, W. Sechrest, E. H. Boakes, C. Carbone, et al. 2009. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology 90:2648.
23. Klingenberg, C. P. 2004. Integration, modules and development: molecules to morphology to evolution. Pp. 213-230 in M. Pigliucci and K. Preston, eds. Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford Univ. Press, Oxford, U.K.
24. Klingenberg, C. P. 2009. Morphometric integration and modularity in configurations of landmarks: tools for evaluating a priori hypotheses. Evol. Dev. 11:405-421.
25. Lande, R. 1979. Quantitative genetic analysis of multivariate evolution applied to brain:body size allometry. Evolution 33:402-416.
26. Lessels, C. M., and P. T. Boag, 1987. Unrepeatable repeatabilities: a common mistake. Auk 104:116-121.
27. Lindenfors, P., J. L. Gittleman, and K. E. Jones 2007. Sexual size dimorphism in mammals. Pp. 16-26 in D. J. Fairbairn, W. U. Blanckenhorn, and T. Szekely, eds. Sex, size and gender roles: evolutionary studies of sexual size dimorphism. Oxford Univ. Press, Oxford, U.K.
28. De Magalhães, J. P., and J. Costa 2009. A database of vertebrate longevity records and their relation to other life-history traits. J. Evol. Biol. 22:1770-1774.
29. Marroig, G., and J. M. Cheverud 2001. A comparison of phenotypic variation and covariation patterns and the role of phylogeny, ecology, and ontogeny during cranial evolution of New World monkeys. Evolution 55:2576-2600.
30. Marroig, G., and J. M. Cheverud 2004a. Cranial evolution in sakis (Pithecia, Platyrrhini) I: Interspecific differentiation and allometric patterns. Am. J. Phys. Anthrop. 125:266-278.
31. Marroig, G., and J. M. Cheverud 2004b. Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? Am. Nat. 163:417-428.
32. Marroig, G., and J. M. Cheverud 2005. Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World Monkeys. Evolution 59:1128-1142.
33. Marroig, G., and J. M. Cheverud 2010. Size as a line of least resistance II: direct selection on size or correlated response due to constraints? Evolution 64:1470-1488.
34. Marroig, G., M. de Vivo, and J. M. Cheverud 2004. Cranial evolution in sakis (Pithecia, Platyrrhini) II: evolutionary processes and morphological integration. J Evol Biol. 17:144-155.
35. Marroig, G., L. T. Shirai, A. Porto, F. B. Oliveira, and V. De Conto 2009. The evolution of modularity in the mammalian skull II: evolutionary consequences. Evol. Biol. 36:136-148.
36. Marroig, G., D. A. R. Melo, and G. Garcia 2012. Modularity, noise and natural selection. Evolution 66:1506-1524.
37. Martínez-Abadías, N., M. Esparza, T. Sjøvold, R. González-José, M. Santos, M. Hernández, and C. P. Klingenberg 2011. Pervasive genetic integration directs the evolution of human skull shape. Evolution 66:1010-1023.
38. Maynard Smith, J., R. Burian, S. Kauffman, P. Alberch, J. Campbell, B. Goodwin, R. Lande, D. Raup, and L. Wolpert 1985. Developmental constraints and evolution: a perspective from the Mountain Lake Conference on Development and Evolution. Quart Rev. Biol. 60:265-287.
39. Mitteroecker, P., and F. Bookstein 2007. The evolutionary role of modularity and integration in the hominoid cranium. Evolution 62:943-958.
40. Monteiro, L. R., V. Bonato, and S. F. dos Reis 2005. Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae). Evol. Dev. 7:429-39.
41. Moore, W. J. 1981. The mammalian skull. Cambridge Univ. Press, Cambridge, U.K.
42. Nijhout, H. F. 2011. Dependence of morphometric allometries on the growth kinetics of body parts. J. Theor. Biol. 288:35-43.
43. Oliveira, F. B., A. Porto, and G. Marroig 2009. Covariance structure in the skull of Catarrhini: a case of pattern stasis and magnitude evolution. J. Human Evol. 56:417-430.
44. Olson, E. C., and R. L. Miller 1958. Morphological integration. University of Chicago Press, Chicago, IL.
45. Pavlicev, M., J. P. Kenney-Hunt, E. A. Norgard, C. C. Roseman, J. B. Wolf, and J. M. Cheverud 2007. Genetic variation in pleiotropy: differential epistasis as a source of variation in the allometric relationship between long bone lengths and body weight. Evolution 62:199-213.
46. Pavlicev, M., E. A. Norgard, G. L. Fawcett, and J. M. Cheverud 2011. Evolution of pleiotropy: epistatic interaction pattern supports a mechanistic model underlying variation in genotype-phenotype map. J. Exp. Zool. 316B:371-385.
47. Porto, A., F. B. Oliveira, L. T. Shirai, V. De Conto, and G. Marroig 2009. The evolution of modularity in the mammalian skull I: morphological integration patterns and magnitudes. Evol. Biol. 36:118-135.
48. Promislow, D. E. L., and P. H. Harvey 1990. Living fast and dying young: a comparative analysis of life-history variation among mammals. J. Zool. 220:417-437.
49. Read, A. F., and P. H. Harvey 1989. Life history differences among the Eutherian radiations. J. Zool. 219:329-353.
50. Schlosser, G., and G. P. Wagner, eds. 2004. Modularity in development and evolution. University of Chicago Press, Chicago, IL.
51. Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50:1766-1774.
52. Shirai, L. T., and G. Marroig 2010. Skull modularity in neotropical marsupials and monkeys: size variation and evolutionary constraint and flexibility. J. Exp. Zool. 314B:663-683.
53. Smith, K. K. 1996. Integration of craniofacial structures during development in mammals. Am. Zool. 36:70-79.
54. Smith, K. K.. 1997. Comparative patterns of craniofacial development in Eutherian and Metatherian mammals. Evolution 51:1663-1678.
55. Smith, K. K.. 2001. Early development of the neural plate, neural crest and facial region of marsupials. J. Anat. 199:121-131.
56. Steppan, S. J., P. C. Phillips, and D. Houle 2002. Comparative quantitative genetics: evolution of the G matrix. Trends Ecol. Evol. 17(7):320-327.
57. Wagner, G. P., and L. Altenberg 1996. Complex adaptations and the evolution of evolvability. Evolution 50:967-976.
58. West, G. B., J. H. Brown, and B. J. Enquist 2001. A general model for ontogenetic growth. Nature 413:628-631.
59. Wilson, D. E., and D. M. Reeder, eds. 2005. Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins Univ. Press, Baltimore, MD.
60. Young, N. M., G. P. Wagner, and B. Hallgrímsson 2010. Development and the evolvability of human limbs. Proc. Nat. Acad. Sci. 107:3400-3405.