On the Relationship between Ontogenetic and Static Allometry

Pélabon, Christophe; Bolstad, Geir H.; Egset, Camilla Kalvatn; Cheverud, James M.; Pavličev, Mihaela; Rosenqvist, Gunilla

doi:10.1086/668820

Cited by 106 publications

(139 citation statements)

References 56 publications

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“…If the genetic variation in SSD we documented here reflects the general pattern in Drosophila, the SSD variation with body size observed among Drosophila species (Blanckenhorn et al, 2007b;Huey et al, 2006) is unlikely to be a mere by-product of body size evolution within species; instead our results suggest that natural selection might directly act on dimorphism itself, as intra-specific patterns, and thus presumably mechanisms, do not predict inter-specific patterns of SSD. The problem is akin to the relationship between ontogenetic and static allometry, which do not necessarily have to be congruent (Cheverud, 1982;Pelabon et al, 2013). However, as genetic variation in the current study was artificially introduced by using a collection of isogenic deficiencies, we cannot be sure that it actually reflects natural genetic variation in Drosophila.…”

Section: Discussionmentioning

confidence: 93%

Effect of genomic deficiencies on sexual size dimorphism through modification of developmental time in Drosophila melanogaster

Takahashi

Blanckenhorn

2015

Heredity

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Sexual size dimorphism (SSD), a difference in body size between sexes, is common in many taxa. In insects, females are larger than males in 470% of all taxa in most orders. The fruit fly, Drosophila melanogaster is one prominent model organism to investigate SSD since its clear and representative female-biased SSD and its growth regulation are well studied. Elucidating the number and nature of genetic elements that can potentially influence SSD would be helpful in understanding the evolutionary potential of SSD. Here, we investigated the SSD pattern caused by artificially introduced genetic variation in D. melanogaster, and examined whether variation in SSD was mediated by the sex-specific modification of developmental time. To map the genomic regions that had effects on sexual wing size and/or developmental time differences (SDtD), we reanalyzed previously published genome-wide deficiency mapping data to evaluate the effects of 376 isogenic deficiencies covering a total of~67% of the genomic regions of the second and third chromosomes of D. melanogaster. We found genetic variation in SSD and SDtD generated by genomic deficiencies, and a negative genetic correlation between size and development time. We also found SSD and SDtD allometries that are not qualitatively congruent, which however overall at best only partly help in explaining the patterns found. We identified several genomic deficiencies with the tendency to either exaggerate or suppress SSD, in agreement with quantitative genetic null expectations of many loci with small effects. These novel findings contribute to a better understanding of the evolutionary potential of sexual dimorphism.

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Section: Discussionmentioning

confidence: 93%

Effect of genomic deficiencies on sexual size dimorphism through modification of developmental time in Drosophila melanogaster

Takahashi

Blanckenhorn

2015

Heredity

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“…These individual growth parameters can be expressed as individual allometries that relate to the static allometry in the same way as ontogenetic allometries (see ref. 23). Under this model, individuals that are near the bivariate phenotypic mean (i.e., average wing size and vein length) could have any breeding value for slope, and selection of those individuals would contribute nothing to the selection differential for slope.…”

Section: Resultsmentioning

confidence: 99%

“…Allometric power laws summarize variation among developmental stages (ontogenetic allometry), individuals in a population (static allometry), and populations or species (evolutionary allometry) (22). The three levels of allometry are related, and a higher level of allometry can be expressed as a function of allometry at lower levels (23). Limited potential for evolution at a lower level in this allometric hierarchy would then cause constraints at all higher levels (6,23).…”

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confidence: 99%

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Complex constraints on allometry revealed by artificial selection on the wing ofDrosophila melanogaster

Bolstad

Cassara

Márquez

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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118

170

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Precise exponential scaling with size is a fundamental aspect of phenotypic variation. These allometric power laws are often invariant across taxa and have long been hypothesized to reflect developmental constraints. Here we test this hypothesis by investigating the evolutionary potential of an allometric scaling relationship in drosophilid wing shape that is nearly invariant across 111 species separated by at least 50 million years of evolution. In only 26 generations of artificial selection in a population of Drosophila melanogaster, we were able to drive the allometric slope to the outer range of those found among the 111 sampled species. This response was rapidly lost when selection was suspended. Only a small proportion of this reversal could be explained by breakup of linkage disequilibrium, and direct selection on wing shape is also unlikely to explain the reversal, because the more divergent wing shapes produced by selection on the allometric intercept did not revert. We hypothesize that the reversal was instead caused by internal selection arising from pleiotropic links to unknown traits. Our results also suggest that the observed selection response in the allometric slope was due to a component expressed late in larval development and that variation in earlier development did not respond to selection. Together, these results are consistent with a role for pleiotropic constraints in explaining the remarkable evolutionary stability of allometric scaling.llometric scaling is a ubiquitous aspect of biological variation that is often strongly conserved across evolutionary time and typically explains a large fraction of observed variation in morphology, physiology, or life history (1-7). This evolutionary conservatism can be explained either by stabilizing selection or by developmental or physiological constraints (8-17). Allometric power laws have been thought to reflect developmental constraints for nearly a century (6). Arguments of allometric constraints were used to explain patterns of macroevolution by architects of the modern synthesis such as Huxley (5), Simpson (18), and Rensch (19), and played a major role in Gould and Lewontin's (20) criticism of the "adaptationist programme." The idea of allometric constraints may, at least partially, have originated from the multiplicative growth model underlying Huxley's derivation of the allometric power law for morphological traits.Julian Huxley (5, 21) showed that when a trait is under common growth regulation with size, the relationship between the trait Y and a size measure X is a power function of the form Y = aX b , where a and b are constants. On a log-log scale, power functions become linear, with log(a) representing the intercept and b representing the slope of the allometric relationship log(Y) = log(a) + b log(X). Allometric power laws summarize variation among developmental stages (ontogenetic allometry), individuals in a population (static allometry), and populations or species (evolutionary allometry) (22). The three levels of allometry are relat...

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“…Ontogenetic allometry is associated with size increase due to growth in individuals of a single species, evolutionary allometry is associated with size differences among species and static allometry is due to variation of size within a population and in a single growth stage. A variety of comparisons have been made across levels of allometry [30][31][32], increasingly with the new methods of geometric morphometrics [25,[33][34][35]. These comparisons across levels of allometry can serve as models for analyses of morphological integration and modularity.…”

Section: Introductionmentioning

confidence: 99%

Studying morphological integration and modularity at multiple levels: concepts and analysis

Klingenberg

2014

Phil. Trans. R. Soc. B

289

301

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Although most studies on integration and modularity have focused on variation among individuals within populations or species, this is not the only level of variation for which integration and modularity exist. Multiple levels of biological variation originate from distinct sources: genetic variation, phenotypic plasticity resulting from environmental heterogeneity, fluctuating asymmetry from random developmental variation and, at the interpopulation or interspecific levels, evolutionary change. The processes that produce variation at all these levels can impart integration or modularity on the covariance structure among morphological traits. In turn, studies of the patterns of integration and modularity can inform about the underlying processes. In particular, the methods of geometric morphometrics offer many advantages for such studies because they can characterize the patterns of morphological variation in great detail and maintain the anatomical context of the structures under study. This paper reviews biological concepts and analytical methods for characterizing patterns of variation and for comparing across levels. Because research comparing patterns across level has only just begun, there are relatively few results, generalizations are difficult and many biological and statistical questions remain unanswered. Nevertheless, it is clear that research using this approach can take advantage of an abundance of new possibilities that are so far largely unexplored.

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On the Relationship between Ontogenetic and Static Allometry

Cited by 106 publications

References 56 publications

Effect of genomic deficiencies on sexual size dimorphism through modification of developmental time in Drosophila melanogaster

Effect of genomic deficiencies on sexual size dimorphism through modification of developmental time in Drosophila melanogaster

Complex constraints on allometry revealed by artificial selection on the wing ofDrosophila melanogaster

Studying morphological integration and modularity at multiple levels: concepts and analysis

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