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 between
Microgeographic adaptation provides a particularly interesting context for understanding the genetic basis of phenotypic divergence and may also present unique empirical challenges. In particular, plant adaptation to extreme soil mosaics may generate barriers to gene flow or shifts in mating system that confound simple genomic scans for adaptive loci. Here, we combine three approaches – quantitative trait locus (QTL) mapping of candidate intervals in controlled crosses, population resequencing (PoolSeq) and analyses of wild recombinant individuals – to investigate one trait associated with
- NSF-PAR ID:
- 10246885
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 25
- Issue:
- 22
- ISSN:
- 0962-1083
- Page Range / eLocation ID:
- p. 5647-5662
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
Abstract Mimulus laciniatus and 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 denseSNP markers across the genome and map quantitative trait loci (QTL s) involved in flowering time, flower size and leaf shape. We find that interspecific divergence in all three traits is due to fewQTL of large effect including a highly pleiotropicQTL on chromosome 8. ThisQTL region contains the pleiotropic candidate gene TCP4 and is involved in ecologically important phenotypes in otherMimulus species. 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. -
Abstract Atlantic killifish (
Fundulus heteroclitus ) residing in some urban and industrialized estuaries of theUS eastern seaboard demonstrate recently evolved and extreme tolerance to toxic aryl hydrocarbon pollutants, characterized as dioxin‐like compounds (DLC s). Here, we provide an unusually comprehensive accounting (69%) through quantitative trait locus (QTL ) analysis of the genetic basis forDLC tolerance in killifish inhabiting an urban estuary contaminated withPCB congeners, the most toxic of which areDLC s. Consistent with mechanistic knowledge ofDLC toxicity in fish and other vertebrates, the aryl hydrocarbon receptor (ahr2 ) region accounts for 17% of trait variation; however,QTL on independent linkage groups and their interactions have even greater explanatory power (44%).QTL interpreted within the context of recently availableFundulus genomic resources and shared synteny among fish species suggest adaptation via interacting components of a complex stress response network. SomeQTL were also enriched in other killifish populations characterized asDLC ‐tolerant and residing in distant urban estuaries contaminated with unique mixtures of pollutants. Together, our results suggest thatDLC tolerance in killifish represents an emerging example of parallel contemporary evolution that has been driven by intense human‐mediated selection on natural populations. -
Abstract Floral attraction traits can significantly affect pollinator visitation patterns, but adaptive evolution of these traits may be constrained by correlations with other traits. In some cases, molecular pathways contributing to floral attraction are well characterized, offering the opportunity to explore loci potentially underlying variation among individuals. Here, we quantify the range of variation in floral
UV patterning (i.e.UV ‘bulls‐eye nectar guides) among crop and wild accessions ofBrassica rapa . We then use experimental crosses to examine the genetic architecture, candidate loci and biochemical underpinnings of this patterning as well as phenotypic manipulations to test the ecological impact. We find qualitative variation inUV patterning between wild (commonly lackingUV patterns) and crop (commonly exhibitingUV patterns) accessions. Similar to the majority of crops, recombinant inbred lines (RIL s) derived from an oilseed crop ×WI fast‐plant®cross exhibitUV patterns, the size of which varies extensively among genotypes. InRIL s, we further observe strong statistical‐genetic andQTL correlations within petal morphological traits and within measurements of petalUV patterning; however, correlations between morphology andUV patterning are weak or nonsignificant, suggesting thatUV patterning is regulated and may evolve independently of overall petal size.HPLC analyses reveal a high concentration of sinapoyl glucose inUV ‐absorbing petal regions, which, in concert with physical locations ofUV ‐traitQTL s, suggest a regulatory and structural gene as candidates underlying observed quantitative variation. Finally, insects prefer flowers withUV bulls‐eye patterns over those that lack patterns, validating the importance ofUV patterning in pollen‐limited populations ofB. rapa . -
Abstract Copy number variation (
CNV ) is a major part of the genetic diversity segregating within populations, but remains poorly understood relative to single nucleotide variation. Here, we report on atRNA ligase gene (Migut.N02091;RLG 1a) exhibiting unprecedented, and fitness‐relevant,CNV within an annual population of the yellow monkeyflowerMimulus guttatus .RLG 1a variation was associated with multiple traits in pooled population sequencing (PoolSeq) scans of phenotypic and phenological cohorts. Resequencing of inbred lines revealed intermediate‐frequency three‐copy variants ofRLG 1a (trip+; 5/35 = 14%), andtrip+ lines exhibited elevatedRLG 1a expression under multiple conditions.trip+ carriers, in addition to being over‐represented in late‐flowering and large‐flowered PoolSeq populations, flowered later under stressful conditions in a greenhouse experiment (p < 0.05). In wild population samples, we discovered an additional rareRLG 1a variant (high+ ) that carries 250–300 copies ofRLG 1a totalling ~5.7 Mb (20–40% of a chromosome). In the progeny of ahigh+ carrier, Mendelian segregation of diagnostic alleles andqPCR ‐based copy counts indicate thathigh+ is a single tandem array unlinked to the single‐copyRLG 1a locus. In the wild,high+ carriers had highest fitness in two particularly dry and/or hot years (2015 and 2017; bothp < 0.01), while single‐copy individuals were twice as fecund as eitherCNV type in a lush year (2016:p < 0.005). Our results demonstrate fluctuating selection onCNV s affecting phenological traits in a wild population, suggest that planttRNA ligases mediate stress‐responsive life‐history traits, and introduce a novel system for investigating the molecular mechanisms of gene amplification. -
Summary Genetic correlations among different components of phenotypes, especially those resulting from pleiotropy, can constrain or facilitate trait evolution. These factors could especially influence the evolution of traits that are functionally integrated, such as those comprising the flower. Indeed, pleiotropy is proposed as a main driver of repeated convergent trait transitions, including the evolution of phenotypically similar pollinator syndromes.
We assessed the role of pleiotropy in the differentiation of floral and other reproductive traits between two species –
Jaltomata sinuosa andJ. umbellata (Solanaceae) – that have divergent suites of floral traits consistent with bee and hummingbird pollination, respectively. To do so, we generated a hybrid population and examined the genetic architecture (trait segregation and quantitative trait locus (QTL ) distribution) underlying 25 floral and fertility traits.We found that most floral traits had a relatively simple genetic basis (few, predominantly additive,
QTL s of moderate to large effect), as well as little evidence of antagonistic pleiotropy (few trait correlations andQTL colocalization, particularly between traits of different classes). However, we did detect a potential case of adaptive pleiotropy among floral size and nectar traits.These mechanisms may have facilitated the rapid floral trait evolution observed within
Jaltomata , and may be a common component of rapid phenotypic change more broadly.