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Title: Large genetic divergence underpins cryptic local adaptation across ecological and evolutionary gradients
Environmentally covarying local adaptation is a form of cryptic local adaptation in which the covariance of the genetic and environmental effects on a phenotype obscures the divergence between locally adapted genotypes. Here, we systematically document the magnitude and drivers of the genetic effect (V G ) for two forms of environmentally covarying local adaptation: counter- and cogradient variation. Using a hierarchical Bayesian meta-analysis, we calculated the overall effect size of V G as 1.05 and 2.13 for populations exhibiting countergradient or cogradient variation, respectively. These results indicate that the genetic contribution to phenotypic variation represents a 1.05 to 2.13 s.d. change in trait value between the most disparate populations depending on if populations are expressing counter- or cogradient variation. We also found that while there was substantial variance among abiotic and biotic covariates, the covariates with the largest mean effects were temperature (2.41) and gamete size (2.81). Our results demonstrate the pervasiveness and large genetic effects underlying environmentally covarying local adaptation in wild populations and highlight the importance of accounting for these effects in future studies. more »« less
Joganic, Jessica L.; Willmore, Katherine E.; Richtsmeier, Joan T.; Weiss, Kenneth M.; Mahaney, Michael C.; Rogers, Jeffrey; Cheverud, James M.(
, American Journal of Physical Anthropology)
AbstractObjectives
Determining the genetic architecture of quantitative traits and genetic correlations among them is important for understanding morphological evolution patterns. We address two questions regarding papionin evolution: (1) what effect do body and cranial size, age, and sex have on phenotypic (VP) and additive genetic (VA) variation in baboon crania, and (2) how might additive genetic correlations between craniofacial traits and body mass affect morphological evolution?
Materials and Methods
We use a large captive pedigreed baboon sample to estimate quantitative genetic parameters for craniofacial dimensions (EIDs). Our models include nested combinations of the covariates listed above. We also simulate the correlated response of a given EID due to selection on body mass alone.
Results
Covariates account for 1.2–91% of craniofacialVP. EIDVAdecreases across models as more covariates are included. The median genetic correlation estimate between each EID and body mass is 0.33. Analysis of the multivariate response to selection reveals that observed patterns of craniofacial variation in extant baboons cannot be attributed solely to correlated response to selection on body mass, particularly in males.
Discussion
Because a relatively large proportion of EIDVAis shared with body mass variation, different methods of correcting for allometry by statistically controlling for size can alter residualVPpatterns. This may conflate direct selection effects on craniofacial variation with those resulting from a correlated response to body mass selection. This shared genetic variation may partially explain how selection for increased body mass in two different papionin lineages produced remarkably similar craniofacial phenotypes.
Farleigh, Keaka; Vladimirova, Sarah A.; Blair, Christopher; Bracken, Jason T.; Koochekian, Nazila; Schield, Drew R.; Card, Daren C.; Finger, Nicholas; Henault, Jonathan; Leaché, Adam D.; et al(
, Molecular Ecology)
Abstract
Species often experience spatial environmental heterogeneity across their range, and populations may exhibit signatures of adaptation to local environmental characteristics. Other population genetic processes, such as migration and genetic drift, can impede the effects of local adaptation. Genetic drift in particular can have a pronounced effect on population genetic structure during large‐scale geographic expansions, where a series of founder effects leads to decreases in genetic variation in the direction of the expansion. Here, we explore the genetic diversity of a desert lizard that occupies a wide range of environmental conditions and that has experienced post‐glacial expansion northwards along two colonization routes. Based on our analyses of a large SNP data set, we find evidence that both climate and demographic history have shaped the genetic structure of populations. Pronounced genetic differentiation was evident between populations occupying cold versus hot deserts, and we detected numerous loci with significant associations with climate. The genetic signal of founder effects, however, is still present in the genomes of the recently expanded populations, which comprise subsets of genetic variation found in the southern populations.
Identifying the environmental correlates of divergence in functional traits between populations can provide insights into the evolutionary mechanisms that generate local adaptation. Here, we assess patterns of population differentiation in expressed venom proteins in Northern Pacific rattlesnakes (Crotalus oreganus) from 13 locations across California. We evaluate the relative importance of major biotic (prey species community composition), abiotic (temperature, precipitation, and elevation) and genetic factors (genetic distance based on RADseq loci) as correlates of population divergence in venom phenotypes. We found that over half of the variation in venom composition is associated with among-population differentiation for genetic and environmental variables, and that this variation occurred along axes defining previously observed functional trade-offs between venom proteins that have neurotoxic, myotoxic and hemorrhagic effects. Surprisingly, genetic differentiation among populations was the best predictor of venom divergence, accounting for 46% of overall variation, whereas differences in prey community composition and abiotic factors explained smaller amounts of variation (23% and 19%, respectively). The association between genetic differentiation and venom composition could be due to an isolation-by-distance effect or, more likely, an isolation-by-environment effect where selection against recent migrants is strong, producing a correlation between neutral genetic differentiation and venom differentiation. Our findings suggest that even coarse estimates of prey community composition can be useful in understanding the selection pressures acting on patterns of venom protein expression. Additionally, our results suggest that factors other than adaptation to spatial variation in prey need to be considered when explaining population divergence in venom.
Ferris, Kathleen G.; Barnett, Laryssa L.; Blackman, Benjamin K.; Willis, John H.(
, Molecular Ecology)
Abstract
The genetic architecture of local adaptation has been of central interest to evolutionary biologists since the modern synthesis. In addition to classic theory on the effect size of adaptive mutations by Fisher, Kimura and Orr, recent theory addresses the genetic architecture of local adaptation in the face of ongoing gene flow. This theory predicts that with substantial gene flow between populations local adaptation should proceed primarily through mutations of large effect or tightly linked clusters of smaller effect loci. In this study, we investigate the genetic architecture of divergence in flowering time, mating system‐related traits, and leaf shape betweenMimulus laciniatusand a sympatric population of its close relativeM. guttatus. These three traits are probably involved inM. laciniatus’adaptation to a dry, exposed granite outcrop environment. Flowering time and mating system differences are also reproductive isolating barriers making them ‘magic traits’. Phenotypic hybrids in this population provide evidence of recent gene flow. Using next‐generation sequencing, we generate denseSNPmarkers across the genome and map quantitative trait loci (QTLs) involved in flowering time, flower size and leaf shape. We find that interspecific divergence in all three traits is due to fewQTLof large effect including a highly pleiotropicQTLon chromosome 8. ThisQTLregion contains the pleiotropic candidate gene TCP4 and is involved in ecologically important phenotypes in otherMimulusspecies. Our results are consistent with theory, indicating that local adaptation and reproductive isolation with gene flow should be due to few loci with large and pleiotropic effects.
Ehrlich, Moritz A; Wagner, Dominique N; Oleksiak, Marjorie F; Crawford, Douglas L(
, Genome Biology and Evolution)
Fraser, Bonnie
(Ed.)
Abstract Selection on standing genetic variation may be effective enough to allow for adaptation to distinct niche environments within a single generation. Minor allele frequency changes at multiple, redundant loci of small effect can produce remarkable phenotypic shifts. Yet, demonstrating rapid adaptation via polygenic selection in the wild remains challenging. Here we harness natural replicate populations that experience similar selection pressures and harbor high within-, yet negligible among-population genetic variation. Such populations can be found among the teleost Fundulus heteroclitus that inhabits marine estuaries characterized by high environmental heterogeneity. We identify 10,861 single nucleotide polymorphisms in F. heteroclitus that belong to a single, panmictic population yet reside in environmentally distinct niches (one coastal basin and three replicate tidal ponds). By sampling at two time points within a single generation, we quantify both allele frequency change within as well as spatial divergence among niche subpopulations. We observe few individually significant allele frequency changes yet find that the “number” of moderate changes exceeds the neutral expectation by 10–100%. We find allele frequency changes to be significantly concordant in both direction and magnitude among all niche subpopulations, suggestive of parallel selection. In addition, within-generation allele frequency changes generate subtle but significant divergence among niches, indicative of local adaptation. Although we cannot distinguish between selection and genotype-dependent migration as drivers of within-generation allele frequency changes, the trait/s determining fitness and/or migration likelihood appear to be polygenic. In heterogeneous environments, polygenic selection and polygenic, genotype-dependent migration offer conceivable mechanisms for within-generation, local adaptation to distinct niches.
Sparks, Morgan M., Kraft, Joshua C., Blackstone, Kliffi M., McNickle, Gordon G., and Christie, Mark R. Large genetic divergence underpins cryptic local adaptation across ecological and evolutionary gradients. Retrieved from https://par.nsf.gov/biblio/10406473. Proceedings of the Royal Society B: Biological Sciences 289.1984 Web. doi:10.1098/rspb.2022.1472.
Sparks, Morgan M., Kraft, Joshua C., Blackstone, Kliffi M., McNickle, Gordon G., & Christie, Mark R. Large genetic divergence underpins cryptic local adaptation across ecological and evolutionary gradients. Proceedings of the Royal Society B: Biological Sciences, 289 (1984). Retrieved from https://par.nsf.gov/biblio/10406473. https://doi.org/10.1098/rspb.2022.1472
Sparks, Morgan M., Kraft, Joshua C., Blackstone, Kliffi M., McNickle, Gordon G., and Christie, Mark R.
"Large genetic divergence underpins cryptic local adaptation across ecological and evolutionary gradients". Proceedings of the Royal Society B: Biological Sciences 289 (1984). Country unknown/Code not available. https://doi.org/10.1098/rspb.2022.1472.https://par.nsf.gov/biblio/10406473.
@article{osti_10406473,
place = {Country unknown/Code not available},
title = {Large genetic divergence underpins cryptic local adaptation across ecological and evolutionary gradients},
url = {https://par.nsf.gov/biblio/10406473},
DOI = {10.1098/rspb.2022.1472},
abstractNote = {Environmentally covarying local adaptation is a form of cryptic local adaptation in which the covariance of the genetic and environmental effects on a phenotype obscures the divergence between locally adapted genotypes. Here, we systematically document the magnitude and drivers of the genetic effect (V G ) for two forms of environmentally covarying local adaptation: counter- and cogradient variation. Using a hierarchical Bayesian meta-analysis, we calculated the overall effect size of V G as 1.05 and 2.13 for populations exhibiting countergradient or cogradient variation, respectively. These results indicate that the genetic contribution to phenotypic variation represents a 1.05 to 2.13 s.d. change in trait value between the most disparate populations depending on if populations are expressing counter- or cogradient variation. We also found that while there was substantial variance among abiotic and biotic covariates, the covariates with the largest mean effects were temperature (2.41) and gamete size (2.81). Our results demonstrate the pervasiveness and large genetic effects underlying environmentally covarying local adaptation in wild populations and highlight the importance of accounting for these effects in future studies.},
journal = {Proceedings of the Royal Society B: Biological Sciences},
volume = {289},
number = {1984},
author = {Sparks, Morgan M. and Kraft, Joshua C. and Blackstone, Kliffi M. and McNickle, Gordon G. and Christie, Mark R.},
}
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