From Micro- to macroevolution through equantitative genetic variation: positive evidence from field crickets

Department of Biology, McGill University, Montréal, Québec, H3A 1B1, Canada.
Evolution (Impact Factor: 4.66). 11/2004; 58(10):2287-304. DOI: 10.1554/04-059
Source: PubMed

ABSTRACT Quantitative genetics has been introduced to evolutionary biologists with the suggestion that microevolution could be directly linked to macroevolutionary patterns using, among other parameters, the additive genetic variance/ covariance matrix (G) which is a statistical representation of genetic constraints to evolution. However, little is known concerning the rate and pattern of evolution of G in nature, and it is uncertain whether the constraining effect of G is important over evolutionary time scales. To address these issues, seven species of field crickets from the genera Gryllus and Teleogryllus were reared in the laboratory, and quantitative genetic parameters for morphological traits were estimated from each of them using a nested full-sibling family design. We used three statistical approaches (T method, Flury hierarchy, and Mantel test) to compare G matrices or genetic correlation matrices in a phylogenetic framework. Results showed that G matrices were generally similar across species, with occasional differences between some species. We suggest that G has evolved at a low rate, a conclusion strengthened by the consideration that part of the observed across-species variation in G can be explained by the effect of a genotype by environment interaction. The observed pattern of G matrix variation between species could not be predicted by either morphological trait values or phylogeny. The constraint hypothesis was tested by comparing the multivariate orientation of the reconstructed ancestral G matrix to the orientation of the across-species divergence matrix (D matrix, based on mean trait values). The D matrix mainly revealed divergence in size and, to a much smaller extent, in a shape component related to the ovipositor length. This pattern of species divergence was found to be predictable from the ancestral G matrix in agreement with the expectation of the constraint hypothesis. Overall, these results suggest that the G matrix seems to have an influence on species divergence, and that macroevolution can be predicted, at least qualitatively, from quantitative genetic theory. Alternative explanations are discussed.

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Available from: Derek Roff, Aug 22, 2015
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    • "The predictive power of quantitative genetics and the importance of genetic constraints in dictating patterns and pace of population differentiation depend on the stability of G. However, with recent theoretical and empirical developments, the question has switched from asking whether G is stable (Arnold et al. 2001) to assessing the conditions favouring its stability or influencing its evolution (Steppan et al. 2002; Jones et al. 2003; Begin & Roff 2004; Arnold et al. 2008). Arnold et al. (2008) have recently reviewed the evolutionary models put forth to elucidate the evolution of G-matrices. "
    Quantitative Genetics in the Wild, Edited by Anne Charmantier, Dany Garant, and Loeske E. B. Kruuk, 03/2014: chapter Evolutionary potential and constraints in wild populations: pages 190-208; Oxford University Press.
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    • "In brief, the breeding experiment is based on a full-sibling design, where the genetic component of variation is estimated from the variation among families of full-siblings. Although the crickets were reared at three different temperatures (24 • C, 28 • C, and 32 • C), we pooled all families in this study to maximize the sample size (genetic covariance matrices for other morphological measurements were stable across temperatures; Bégin et al. 2004). An additional factor is that G. firmus is a wing dimorphic species, where some individuals have fully developed hindwings (long-winged morph) and others have reduced, nonfunctional hindwings (short-winged morph; Veazey et al. 1976; Roff 1986). "
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    ABSTRACT: The role of developmental and genetic integration for evolution is contentious. One hypothesis states that integration acts as a constraint on evolution, whereas an alternative is that developmental and genetic systems evolve to match the functional modularity of organisms. This study examined a morphological structure, the cricket wing, where developmental and functional modules are discordant, making it possible to distinguish the two alternatives. Wing shape was characterized with geometric morphometrics, quantitative genetic information was extracted using a full-sibling breeding design, and patterns of developmental integration were inferred from fluctuating asymmetry of wing shape. The patterns of genetic, phenotypic, and developmental integration were clearly similar, but not identical. Heritabilities for different shape variables varied widely, but no shape variables were devoid of genetic variation. Simulated selection for specific shape changes produced predicted responses with marked deflections due to the genetic covariance structure. Three hypotheses of modularity according to the wing structures involved in sound production were inconsistent with the genetic, phenotypic, or developmental covariance structure. Instead, there appears to be strong integration throughout the wing. The hypothesis that genetic and developmental integration evolve to match functional modularity can therefore be rejected for this example.
    Evolution 10/2010; 64(10):2935-51. DOI:10.1111/j.1558-5646.2010.01030.x · 4.66 Impact Factor
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    • "Empirical studies have not clarified the issue; some studies support the notion that (co)variances strongly influence the rate or direction of evolution (e.g., Schluter 1996; Blows and Higgie 2003; Bégin and Roff 2004; Hunt 2007) whereas others argue against it (e.g., Merilä and Björklund 1999; Badyaev and Hill 2000; McGuigan et al. 2005; Berner and Blanckenhorn 2006; Berner et al. 2008). A major difficulty here is that information on the adaptive landscape has rarely been incorporated and hence it often remains uncertain whether diversification has been driven by selection. "
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    ABSTRACT: How does natural selection shape the structure of variance and covariance among multiple traits, and how do (co)variances influence trajectories of adaptive diversification? We investigate these pivotal but open questions by comparing phenotypic (co)variances among multiple morphological traits across 18 derived lake-dwelling populations of threespine stickleback, and their marine ancestor. Divergence in (co)variance structure among populations is striking and primarily attributable to shifts in the variance of a single key foraging trait (gill raker length). We then relate this divergence to an ecological selection proxy, to population divergence in trait means, and to the magnitude of sexual dimorphism within populations. This allows us to infer that evolution in (co)variances is linked to variation among habitats in the strength of resource-mediated disruptive selection. We further find that adaptive diversification in trait means among populations has primarily involved shifts in gill raker length. The direction of evolutionary trajectories is unrelated to the major axes of ancestral trait (co)variance. Our study demonstrates that natural selection drives both means and (co)variances deterministically in stickleback, and strongly challenges the view that the (co)variance structure biases the direction of adaptive diversification predictably even over moderate time spans.
    Evolution 02/2010; 64(8):2265-77. DOI:10.1111/j.1558-5646.2010.00982.x · 4.66 Impact Factor
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