The degree to which developmental systems bias the phenotypic effects of environmental and genetic variation, and how these biases affect evolution, is subject to much debate. Here, we assess whether developmental variability in beetle horn shape aligns with the phenotypic effects of plasticity and evolutionary divergence, yielding three salient results. First, we find that most pathways previously shown to regulate horn length also affect shape. Second, we find that the phenotypic effects of manipulating divergent developmental pathways are correlated with each other as well as multivariate fluctuating asymmetry—a measure of developmental variability. Third, these effects further aligned with thermal plasticity, population differences and macroevolutionary divergence between sister taxa and more distantly related species. Collectively, our results support the hypothesis that changes in horn shape—whether brought about by environmentally plastic responses, functional manipulations or evolutionary divergences—converge along ‘developmental lines of least resistance’, i.e. are biased by the developmental system underpinning horn shape.
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A common mechanism drives the alignment between the micro‐ and macroevolution of primate molars
A central challenge for biology is to reveal how different levels of biological variation interact and shape diversity. However, recent experimental studies have indicated that prevailing models of evolution cannot readily explain the link between micro- and macroevolution at deep timescales. Here, we suggest that this paradox could be the result of a common mechanism driving a correlated pattern of evolution. We examine the proportionality between genetic variance and patterns of trait evolution in a system whose developmental processes are well understood to gain insight into how such alignment between morphological divergence and genetic variation might be maintained over macroevolutionary time. Primate molars present a model system by which to link developmental processes to evolutionary dynamics because of the biased pattern of variation that results from the developmental architecture regulating their formation. We consider how this biased variation is expressed at the population level, and how it manifests through evolution across primates. There is a strong correspondence between the macroevolutionary rates of primate molar divergence and their genetic variation. This suggests a model of evolution in which selection is closely aligned with the direction of genetic variance, phenotypic variance, and the underlying developmental architecture of anatomical traits.
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- Award ID(s):
- 1942717
- NSF-PAR ID:
- 10388829
- Date Published:
- Journal Name:
- Evolution
- Volume:
- 76
- Issue:
- 12
- ISSN:
- 0014-3820
- Page Range / eLocation ID:
- 2975-2985
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Macroevolutionary biologists have classically rejected the notion that higher-level patterns of divergence arise through microevolutionary processes acting within populations. For morphology, this consensus partly derives from the inability of quantitative genetics models to correctly predict the behaviour of evolutionary processes at the scale of millions of years. Developmental studies (evo-devo) have been proposed to reconcile micro- and macroevolution. However, there has been little progress in establishing a formal framework to apply evo-devo models of phenotypic diversification. Here we reframe this issue by asking whether using evo-devo models to quantify biological variation can improve the explanatory power of comparative models, thus helping us bridge the gap between micro- and macroevolution. We test this prediction by evaluating the evolution of primate lower molars in a comprehensive dataset densely sampled across living and extinct taxa. Our results suggest that biologically informed morphospaces alongside quantitative genetics models allow a seamless transition between the micro- and macroscales, whereas biologically uninformed spaces do not. We show that the adaptive landscape for primate teeth is corridor like, with changes in morphology within the corridor being nearly neutral. Overall, our framework provides a basis for integrating evo-devo into the modern synthesis, allowing an operational way to evaluate the ultimate causes of macroevolution.more » « less
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Abstract Objectives The objectives of this study are to describe genetic correlations between dental dimensions in a platyrrhine primate, to assess whether the brown‐mantled tamarin dentition exhibits genetic modularity by tooth type, and to discuss the relationship between body size reduction and the genetic architecture of dental traits.
Materials and methods Genetic correlations were estimated for linear dental measurements, estimated crown areas, and measures of relative premolar and molar size from 302 individuals, using a pedigree of 386 individuals, with maximum likelihood variance decomposition in SOLAR.
Results Genetic correlation estimates indicate strong genetic integration in the dentition of brown‐mantled tamarins, with little evidence of modularity by tooth type, within and between the maxilla and mandible. The relative molar size variable hypothesized to be genetically patterned in baboons is not significantly heritable, and relative premolar size does not meet the criteria to be considered genetically patterned in this population.
Discussion These results demonstrate variation in the pattern of genetic correlations between dental dimensions in primates, providing evidence of evolution of the genetic architecture in the callitrichine lineage. Genetic integration of dental dimensions without modularity by tooth type, as demonstrated here, is expected to constrain dental evolution in ways that modularity would not. The role of body size reduction in the callitrichine lineage in the evolution of the genetic architecture of the dentition is discussed. Quantitative genetic analyses of dental dimensions in more primate populations will provide greater evidence of variation and evolution in the genetic architecture underlying primate dental morphology.
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Abstract The evolution of sexual dimorphisms requires divergence between sexes in the evolutionary trajectories of the traits involved. Discerning how genetic architecture could facilitate such divergence has proven challenging because of the difficulty in estimating non-additive and sex-linked genetic variances using traditional quantitative genetic designs. Here we use a three-generation, double-first-cousin pedigree design to estimate additive, sex-linked and dominance (co)variances for 12 traits in the water strider,
Aquarius remigis . Comparisons among these traits, which have size ratios ranging from 1 to 5 (larger/smaller), allow us to ask if sexual dimorphisms are associated with characteristic patterns of quantitative genetic variation. We frame our analysis around three main questions, derived from existing theory and empirical evidence: Are sexual dimorphisms associated with (1) lower additive inter-sex genetic correlations, (2) higher proportions of sex-linked variance, or (3) differences between sexes in autosomal additive and dominance genetic variances? For questions (1) and (2), we find weak and non-significant trends in the expected directions, which preclude definitive conclusions. However, in answer to question (3), we find strong evidence for a positive relationship between sexual dimorphism and differences between sexes in proportions of autosomal dominance variance. We also find strong interactions among the three genetic components indicating that their relative influence differs among traits and between sexes. These results highlight the need to include all three components of genetic (co)variance in both theoretical evolutionary models and empirical estimations of the genetic architecture of dimorphic traits. -
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Abstract Sexual signalling traits are often observed to diverge rapidly among populations, thereby playing a potentially key early role in the evolution of reproductive isolation. While often assumed to reflect divergent sexual selection among populations, patterns of sexual trait diversification might sometimes be biased along axes of standing additive genetic variation and covariation among trait components. Additionally, theory predicts that environmentally induced phenotypic variation might facilitate rapid trait evolution, suggesting that patterns of divergence between populations should mirror phenotypic plasticity within populations. Here, we evaluate the concordance between observed axes of multivariate sexual trait divergence and predicted divergence based on (1) interpopulation variation in sexual selection, (2) additive genetic variances and (3) temperature‐related phenotypic plasticity in male courtship song among geographically isolated populations of the Hawaiian swordtail cricket,
Laupala cerasina , which exhibit sexual isolation due acoustic signalling traits. The major axis of multivariate divergence,d max, accounted for 76% of variation among population male song trait means and was moderately correlated with interpopulation differences in directional sexual selection based on female preferences. However, the majority of additive genetic variance was largely oriented away from the direction of divergence, suggesting that standing genetic variation may not play a dominant role in the patterning of signal divergence. In contrast, the axis of phenotypic plasticity strongly mirrored patterns of interpopulation phenotypic divergence, which is consistent with a role for temperature‐related plasticity in facilitating instead of inhibiting male song evolution and sexual isolation in these incipient species. We propose potential mechanisms by which sexual selection might interact with phenotypic plasticity to facilitate the rapid acoustic diversification observed in this species and clade.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1111/evo.14600
