Cryptic Genetic Variation in Natural Populations: A Predictive Framework

Abstract How new discrete states of morphological traits evolve is poorly understood. One possibility is that single-gene changes underlie the evolution of new discrete character states and that evolution is dependent on the occurrence of new single-gene mutations. Another possibility is that multiple-gene changes are required to elevate an individual or population above a threshold required to produce the new character state. A prediction of the latter model is that genetic variation for the traits should exist in natural populations in the absence of phenotypic variation. To test this idea, we studied traits that are phenotypically invariant within teosinte and for which teosinte is discretely different from its near relative, maize. By employing a QTL mapping strategy to analyze the progeny of a testcross between an F1 of two teosintes and a maize inbred line, we identified cryptic genetic variation in teosinte for traits that are invariant in teosinte. We argue that such cryptic genetic variation can contribute to the evolution of novelty when reconfigured to exceed the threshold necessary for phenotypic expression or by acting to modify or stabilize the effects of major mutations.

Download Full-text

Cryptic genetic variation underpins rapid adaptation to ocean acidification

10.1101/700526 ◽

2019 ◽

Cited By ~ 2

Author(s):

M. C. Bitter ◽

L. Kapsenberg ◽

J.-P. Gattuso ◽

C. A. Pfister

Keyword(s):

Climate Change ◽

Genetic Variation ◽

Natural Populations ◽

Future Climate Change ◽

Rapid Adaptation ◽

Larval Size ◽

Larval Population ◽

Cryptic Genetic Variation ◽

Standing Variation ◽

Seawater Ph

AbstractGlobal climate change has intensified the need to assess the capacity for natural populations to adapt to abrupt shifts in the environment. Reductions in seawater pH constitute a conspicuous stressor associated with increasing atmospheric carbon dioxide that is affecting ecosystems throughout the world’s oceans. Here, we quantify the phenotypic and genetic modifications associated with rapid adaptation to reduced seawater pH in the marine mussel, Mytilus galloprovincialis. We reared a genetically diverse larval population in ambient and extreme low pH conditions (pHT 8.1 and 7.4) and tracked changes in the larval size and allele frequency distributions through settlement. Additionally, we separated larvae by size to link a fitness-related trait to its underlying genetic background in each treatment. Both phenotypic and genetic data show that M. galloprovincialis can evolve in response to a decrease in seawater pH. This process is polygenic and characterized by genotype-environment interactions, suggesting the role of cryptic genetic variation in adaptation to future climate change. Holistically, this work provides insight into the processes underpinning rapid evolution, and demonstrates the importance of maintaining standing variation within natural populations to bolster species’ adaptive capacity as global change progresses.

Download Full-text

C. elegansharbors pervasive cryptic genetic variation for embryogenesis

10.1101/008532 ◽

2014 ◽

Author(s):

Annalise Paaby ◽

Amelia White ◽

David Riccardi ◽

Kristin Gunsalus ◽

Fabio Piano ◽

...

Keyword(s):

Genetic Variation ◽

Gene Networks ◽

Genetic Basis ◽

Disease Susceptibility ◽

Disease Risk ◽

Natural Populations ◽

Cryptic Genetic Variation ◽

Natural Genetic Variation ◽

C Elegans ◽

In The Wild

Conditionally functional mutations are an important class of natural genetic variation, yet little is known about their prevalence in natural populations or their contribution to disease risk. Here, we describe a vast reserve of cryptic genetic variation, alleles that are normally silent but which affect phenotype when the function of other genes is perturbed, in the gene networks ofC. elegansembryogenesis. We find evidence that cryptic-effect loci are ubiquitous and segregate at intermediate frequencies in the wild. The cryptic alleles demonstrate low developmental pleiotropy, in that specific, rather than general, perturbations are required to reveal them. Our findings underscore the importance of genetic background in characterizing gene function and provide a model for the expression of conditionally functional effects that may be fundamental in basic mechanisms of trait evolution and the genetic basis of disease susceptibility.

Download Full-text

Wild worm embryogenesis harbors ubiquitous polygenic modifier variation

eLife ◽

10.7554/elife.09178 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 45

Author(s):

Annalise B Paaby ◽

Amelia G White ◽

David D Riccardi ◽

Kristin C Gunsalus ◽

Fabio Piano ◽

...

Keyword(s):

Genetic Variation ◽

Caenorhabditis Elegans ◽

Gene Function ◽

Natural Populations ◽

Complex Trait ◽

Genetic Modifiers ◽

Wild Type ◽

Cryptic Genetic Variation ◽

Quantitative Genetic ◽

In The Wild

Embryogenesis is an essential and stereotypic process that nevertheless evolves among species. Its essentiality may favor the accumulation of cryptic genetic variation (CGV) that has no effect in the wild-type but that enhances or suppresses the effects of rare disruptions to gene function. Here, we adapted a classical modifier screen to interrogate the alleles segregating in natural populations of Caenorhabditis elegans: we induced gene knockdowns and used quantitative genetic methodology to examine how segregating variants modify the penetrance of embryonic lethality. Each perturbation revealed CGV, indicating that wild-type genomes harbor myriad genetic modifiers that may have little effect individually but which in aggregate can dramatically influence penetrance. Phenotypes were mediated by many modifiers, indicating high polygenicity, but the alleles tend to act very specifically, indicating low pleiotropy. Our findings demonstrate the extent of conditional functionality in complex trait architecture.

Download Full-text

Compensatory evolution via cryptic genetic variation: Distinct trajectories to phenotypic and fitness recovery

10.1101/200725 ◽

2017 ◽

Cited By ~ 3

Author(s):

Sudarshan Chari ◽

Christian Marier ◽

Cody Porter ◽

Emmalee Northrop ◽

Alexandra Belinky ◽

...

Keyword(s):

Genetic Variation ◽

Natural Selection ◽

Allelic Variation ◽

Courtship Behavior ◽

Natural Populations ◽

Wing Morphology ◽

Cryptic Genetic Variation ◽

Compensatory Evolution ◽

Compensatory Adaptation ◽

Deleterious Alleles

AbstractPopulations are constantly exposed to deleterious alleles, most of which are purged via natural selection. However, deleterious fitness effects of alleles can also be suppressed by compensatory adaptation. Compensatory mutations can act directly to reduce deleterious effects of an allele. Alternatively, compensation may also occur by altering other aspects of an organisms’ phenotype or performance, without suppressing the phenotypic effects of the deleterious allele. Moreover, the origin of allelic variation contributing to compensatory adaptation remains poorly understood. Compensatory evolution driven by mutations that arise during the selective process are well studied. However less is known about the role standing (cryptic) genetic variation plays in compensatory adaptation. To address these questions, we examined evolutionary trajectories of natural populations of Drosophila melanogaster fixed for mutations that disrupt wing morphology, resulting in deleterious effects on several components of fitness. Lineages subjected only to natural selection, evolved modifications to courtship behavior and several life history traits without compensation in wing morphology. Yet, we observed rapid phenotypic compensation of wing morphology under artificial selection, consistent with segregating variation for compensatory alleles. We show that alleles contributing to compensation of wing morphology have deleterious effects on other fitness components. These results demonstrate the potential for multiple independent avenues for rapid compensatory adaptation from standing genetic variation, which ultimately may reveal novel adaptive trajectories.

Download Full-text

What maintains genetic variation in natural populations? A commentary on ‘The maintenance of genetic variability by mutation in a polygenic character with linked loci’ by Russell Lande

Genetics Research ◽

10.1017/s0016672308009567 ◽

2007 ◽

Vol 89 (5-6) ◽

pp. 371-372 ◽

Cited By ~ 2

Author(s):

PATRICK C. PHILLIPS

Keyword(s):

Genetic Variation ◽

Genetic Variability ◽

Natural Populations

Download Full-text

POPULATION GENETICS OF ALLOZYME VARIATION IN NEUROSPORA INTERMEDIA

Genetics ◽

10.1093/genetics/80.4.785 ◽

1975 ◽

Vol 80 (4) ◽

pp. 785-805

Author(s):

P T Spieth

Keyword(s):

Genetic Variation ◽

Vegetative Reproduction ◽

Vascular Plant ◽

Natural Populations ◽

Allozyme Variation ◽

Regular Feature ◽

Local Populations ◽

Neurospora Intermedia ◽

Pattern Of Variation ◽

High Level

ABSTRACT Electrophoretically detectable variation in the fungus Neurospora intermedia has been surveyed among isolates from natural populations in Malaya, Papua, Australia and Florida. The principal result is a pattern of genetic variation within and between populations that is qualitatively no different than the well documented patterns for Drosophila and humans. In particular, there is a high level of genetic variation, the majority of which occurs at the level of local populations. Evidence is presented which argues that N. intermedia has a population structure analogous to that of an annual vascular plant with a high level of vegetative reproduction. Sexual reproduction appears to be a regular feature in the biology of the species. Substantial heterokaryon function seems unlikely in natural populations of N. intermedia. Theoretical considerations concerning the mechanisms underlying the observed pattern of variation most likely should be consistent with haploid selection theory. The implications of this constraint upon the theory are discussed in detail, leading to the presentation of a model based upon the concept of environmental heterogeneity. The essence of the model, which is equally applicable to haploid and diploid situations, is a shifting distribution of multiple adaptive niches among local populations such that a given population has a small net selective pressure in favor of one allele or another, depending upon its particular distribution of niches. Gene flow among neighboring populations with differing net selective pressures is postulated as the principal factor underlying intrapopulational allozyme variation.

Download Full-text

Female Genotypes Affect Sperm Displacement in Drosophila

Genetics ◽

10.1093/genetics/149.3.1487 ◽

1998 ◽

Vol 149 (3) ◽

pp. 1487-1493 ◽

Cited By ~ 6

Author(s):

Andrew G Clark ◽

David J Begun

Keyword(s):

Drosophila Melanogaster ◽

Genetic Variation ◽

Natural Populations ◽

Isogenic Line ◽

Female Fitness ◽

Sperm Displacement ◽

Extensive Variation ◽

Polymorphic Genes ◽

Displacement Parameter ◽

Competitive Success

Abstract Differential success of sperm is likely to be an important component of fitness. Extensive variation among male genotypes in competitive success of sperm in multiply mated females has been documented for Drosophila melanogaster. However, virtually all previous studies considered the female to be a passive vessel. Nevertheless, under certain conditions female fitness could be determined by her role in mediating use of sperm from multiple males. Here we ask whether females differ among genotypes in their tendency to exhibit last-male precedence. Competition of sperm from two tester male genotypes (bwD and B3-09, a third-chromosome isogenic line from Beltsville, MD) was quantified by doubly mating female lines that had been rendered homozygous for X, second, or third chromosomes isolated from natural populations. The composite sperm displacement parameter, P2′, was highly heterogeneous among lines, whether or not viability effects were compensated, implying the presence of polymorphic genes affecting access of sperm to eggs. Genetic variation of this type is completely neutral in the absence of pleiotropy or interaction between variation in the two sexes.

Download Full-text

Cryptic genetic variation in a heat shock protein modifies the outcome of a mutation affecting epidermal stem cell development in C. elegans

Nature Communications ◽

10.1038/s41467-021-23567-1 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Sneha L. Koneru ◽

Mark Hintze ◽

Dimitris Katsanos ◽

Michalis Barkoulas

Keyword(s):

Genetic Variation ◽

Stem Cell ◽

Heat Shock ◽

Heat Shock Protein ◽

Cell Fate ◽

Cell Development ◽

Wnt Signalling ◽

Single Amino Acid ◽

Cryptic Genetic Variation ◽

Seam Cell

AbstractA fundamental question in medical genetics is how the genetic background modifies the phenotypic outcome of mutations. We address this question by focusing on the seam cells, which display stem cell properties in the epidermis of Caenorhabditis elegans. We demonstrate that a putative null mutation in the GATA transcription factor egl-18, which is involved in seam cell fate maintenance, is more tolerated in the CB4856 isolate from Hawaii than the lab reference strain N2 from Bristol. We identify multiple quantitative trait loci (QTLs) underlying the difference in phenotype expressivity between the two isolates. These QTLs reveal cryptic genetic variation that reinforces seam cell fate through potentiating Wnt signalling. Within one QTL region, a single amino acid deletion in the heat shock protein HSP-110 in CB4856 is sufficient to modify Wnt signalling and seam cell development, highlighting that natural variation in conserved heat shock proteins can shape phenotype expressivity.

Download Full-text