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Genetic Basis of Phenotypic Variation in Drosophila and Other Insects

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A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (29 February 2020) | Viewed by 37277

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Special Issue Editors

Prof. J. Spencer Johnston

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Guest Editor

Department of Entomology, Texas A&M University, College Station, TX 77843, USA
Interests: genome size evolution; evolution of mobile elements; genomics

Dr. Carl E. Hjelmen

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Guest Editor

Department of Biology, Texas A&M University, College Station, TX 77843, USA
Interests: sex chromosome evolution; heterochromatin; underreplication; genome size

Special Issue Information

Dear Colleagues,

The wealth of genomic sequence data generated on an ever-increasing number of species has no road map. How sequences generate the observed diversity of living forms remains largely unanswered. The diversity in coding sequences is responsible some of this diversity, but the degree to which it contributes is unclear. Coding and non-coding sequences are involved in a network of interactions which can change the level of expression and change the timing of that expression, creating further diversity. Novel phenotypes emerge from these interactions, and the diversity this generates may be further altered by interactions with the environment.

Tools to untangle the sources of diversity have been developed. Most rely upon comparisons of the sequence and phenotypic differences among strains and species. Frequently, these tools take advantage of the sequence quality of the Drosophila genome, the local and global variety of generated Drosophila melanogaster strains, and the even greater range of phenotypes among species in the genus. Adding to this are studies that compare the Drosophila genomic sequence to that of insects with unique phenotypic adaptations. The multiple authors of the Special Issue are among the leaders in this effort, and share their contributions towards generating a road map connecting the gene networks and phenotypic diversity created by genetic and environmental change.

Prof. J. Spencer Johnston
Dr. Carl E. Hjelmen
Guest Editors

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Keywords

gene networks
quantitative genomics
Drosophila strains
Drosophila species
plasticity
local adaptation

Published Papers (11 papers)

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Editorial

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3 pages, 177 KiB

Open AccessEditorial

Special Issue: Genetic Basis of Phenotypic Variation in Drosophila and Other Insects

by J. Spencer Johnston and Carl E. Hjelmen

Genes 2021, 12(8), 1212; https://0-doi-org.brum.beds.ac.uk/10.3390/genes12081212 - 05 Aug 2021

Viewed by 1440

Abstract

Next-generation sequencing provides a nearly complete genomic sequence for model and non-model species alike; however, this wealth of sequence data includes no road map [...] Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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13 pages, 1227 KiB

Open AccessArticle

Comparative Transcriptomics Reveals Gene Families Associated with Predatory Behavior in Photuris femme fatale Fireflies

by Cheyenne N. McKinley and Sarah E. Lower

Genes 2020, 11(6), 627; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11060627 - 07 Jun 2020

Cited by 5 | Viewed by 3071

Abstract

Identifying the basis of phenotypic variation is a key objective of genetics. This work has been mostly limited to model systems with a plethora of genetic manipulation and functional characterization tools. With the development of high-throughput sequencing and new computational tools, it is possible to identify candidate genes related to phenotypic variation in non-model organisms. Fireflies are excellent for studying phenotypic variation because of their diverse and well-characterized behaviors. Most adult fireflies emit a single mating flash pattern and do not eat. In contrast, adult females of many species in the genus Photuris employ multiple flash patterns and prey upon mate-seeking males of other firefly species. To investigate the genetic basis for this variation, we used comparative transcriptomics to identify positively selected genes between a predatory firefly, Photuris sp., and a non-predatory relative, Photuris frontalis, controlling for genes generally under selection in fireflies by comparing to a Photinus firefly. Nine gene families were identified under positive selection in the predatory versus non-predatory Photuris comparison, including genes involved in digestion, detoxification, vision, reproduction, and neural processes. These results generate intriguing hypotheses about the genetic basis for insect behavior and highlight the utility of comparative transcriptomic tools to investigate complex behaviors in non-model systems. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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16 pages, 2093 KiB

Open AccessArticle

Does Divergence in Habitat Breadth Associate with Species Differences in Decision Making in Drosophila sechellia and Drosophila simulans?

by Madeline P. Burns, Frederick D. Cavallaro and Julia B. Saltz

Genes 2020, 11(5), 528; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11050528 - 09 May 2020

Cited by 5 | Viewed by 2690

Abstract

Decision making is involved in many behaviors contributing to fitness, such as habitat choice, mate selection, and foraging. Because of this, high decision-making accuracy (i.e., selecting the option most beneficial for fitness) should be under strong selection. However, decision making is energetically costly, often involving substantial time and energy to survey the environment to obtain high-quality information. Thus, for high decision making accuracy to evolve, its benefits should outweigh its costs. Inconsistency in the net benefits of decision making across environments is hypothesized to be an important means for maintaining variation in this trait. However, very little is known about how environmental factors influence the evolution of decision making to produce variation among individuals, genotypes, and species. Here, we compared two recently diverged species of Drosophila differing substantially in habitat breadth and degree of environmental predictability and variability: Drosophila sechellia and Drosophila simulans. We found that the species evolving under higher environmental unpredictability and variability showed higher decision-making accuracy, but not higher environmental sampling. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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27 pages, 7377 KiB

Open AccessArticle

Combining Experimental Evolution and Genomics to Understand How Seed Beetles Adapt to a Marginal Host Plant

by Alexandre Rêgo, Samridhi Chaturvedi, Amy Springer, Alexandra M. Lish, Caroline L. Barton, Karen M. Kapheim, Frank J. Messina and Zachariah Gompert

Genes 2020, 11(4), 400; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11040400 - 08 Apr 2020

Cited by 7 | Viewed by 3875

Abstract

Genes that affect adaptive traits have been identified, but our knowledge of the genetic basis of adaptation in a more general sense (across multiple traits) remains limited. We combined population-genomic analyses of evolve-and-resequence experiments, genome-wide association mapping of performance traits, and analyses of gene expression to fill this knowledge gap and shed light on the genomics of adaptation to a marginal host (lentil) by the seed beetle Callosobruchus maculatus. Using population-genomic approaches, we detected modest parallelism in allele frequency change across replicate lines during adaptation to lentil. Mapping populations derived from each lentil-adapted line revealed a polygenic basis for two host-specific performance traits (weight and development time), which had low to modest heritabilities. We found less evidence of parallelism in genotype-phenotype associations across these lines than in allele frequency changes during the experiments. Differential gene expression caused by differences in recent evolutionary history exceeded that caused by immediate rearing host. Together, the three genomic datasets suggest that genes affecting traits other than weight and development time are likely to be the main causes of parallel evolution and that detoxification genes (especially cytochrome P450s and beta-glucosidase) could be especially important for colonization of lentil by C. maculatus. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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17 pages, 1556 KiB

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Dissecting the Genetic Basis of Variation in Drosophila Sleep Using a Multiparental QTL Mapping Resource

by Brittny R. Smith and Stuart J. Macdonald

Genes 2020, 11(3), 294; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11030294 - 11 Mar 2020

Cited by 6 | Viewed by 3035

Abstract

There is considerable variation in sleep duration, timing and quality in human populations, and sleep dysregulation has been implicated as a risk factor for a range of health problems. Human sleep traits are known to be regulated by genetic factors, but also by an array of environmental and social factors. These uncontrolled, non-genetic effects complicate powerful identification of the loci contributing to sleep directly in humans. The model system, Drosophila melanogaster, exhibits a behavior that shows the hallmarks of mammalian sleep, and here we use a multitiered approach, encompassing high-resolution QTL mapping, expression QTL data, and functional validation with RNAi to investigate the genetic basis of sleep under highly controlled environmental conditions. We measured a battery of sleep phenotypes in >750 genotypes derived from a multiparental mapping panel and identified several, modest-effect QTL contributing to natural variation for sleep. Merging sleep QTL data with a large head transcriptome eQTL mapping dataset from the same population allowed us to refine the list of plausible candidate causative sleep loci. This set includes genes with previously characterized effects on sleep and circadian rhythms, in addition to novel candidates. Finally, we employed adult, nervous system-specific RNAi on the Dopa decarboxylase, dyschronic, and timeless genes, finding significant effects on sleep phenotypes for all three. The genes we resolve are strong candidates to harbor causative, regulatory variation contributing to sleep. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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22 pages, 4248 KiB

Open AccessArticle

Geographic Life History Differences Predict Genomic Divergence Better than Mitochondrial Barcodes or Phenotype

by Daniel P. Duran, Robert A. Laroche, Harlan M. Gough, Rodger A. Gwiazdowski, Charles B. Knisley, David P. Herrmann, Stephen J. Roman and Scott P. Egan

Genes 2020, 11(3), 265; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11030265 - 29 Feb 2020

Cited by 17 | Viewed by 4738

Abstract

Species diversity can be inferred using multiple data types, however, results based on genetic data can be at odds with patterns of phenotypic variation. Tiger beetles of the Cicindelidia politula (LeConte, 1875) species complex have been taxonomically problematic due to extreme phenotypic variation within and between populations. To better understand the biology and taxonomy of this group, we used mtDNA genealogies and multilocus nuclear analyses of 34,921 SNPs to elucidate its evolutionary history and evaluate the validity of phenotypically circumscribed species and subspecies. Genetic analyses recovered two divergent species that are also ecologically distinct, based on adult life history. These patterns are incongruous with the phenotypic variation that informed prior taxonomy, and most subspecies were not supported as distinct evolutionary lineages. One of the nominal subspecies was found to be a cryptic species; consequently, we elevate C. p. laetipennis (Horn, 1913) to a full species. Although nuclear and mtDNA datasets recovered broadly similar evolutionary units, mito-nuclear discordance was more common than expected, being observed between nearly all geographically overlapping taxonomic pairs. Additionally, a pattern of ‘mitochondrial displacement’ was observed, where mitochondria from one species unidirectionally displace others. Overall, we found that geographically associated life history factors better predict genomic divergence than phenotype and mitochondrial genealogies, and consequently taxon identifications based on mtDNA (e.g., DNA barcodes) may be misleading. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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12 pages, 1724 KiB

Open AccessArticle

Flying High—Muscle-Specific Underreplication in Drosophila

by J. Spencer Johnston, Mary E. Zapalac and Carl E. Hjelmen

Genes 2020, 11(3), 246; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11030246 - 26 Feb 2020

Cited by 4 | Viewed by 2469

Abstract

Drosophila underreplicate the DNA of thoracic nuclei, stalling during S phase at a point that is proportional to the total genome size in each species. In polytene tissues, such as the Drosophila salivary glands, all of the nuclei initiate multiple rounds of DNA synthesis and underreplicate. Yet, only half of the nuclei isolated from the thorax stall; the other half do not initiate S phase. Our question was, why half? To address this question, we use flow cytometry to compare underreplication phenotypes between thoracic tissues. When individual thoracic tissues are dissected and the proportion of stalled DNA synthesis is scored in each tissue type, we find that underreplication occurs in the indirect flight muscle, with the majority of underreplicated nuclei in the dorsal longitudinal muscles (DLM). Half of the DNA in the DLM nuclei stall at S phase between the unreplicated G0 and fully replicated G1. The dorsal ventral flight muscle provides the other source of underreplication, and yet, there, the replication stall point is earlier (less DNA replicated), and the endocycle is initiated. The differences in underreplication and ploidy in the indirect flight muscles provide a new tool to study heterochromatin, underreplication and endocycle control. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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15 pages, 1269 KiB

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The Genetic Basis of Natural Variation in Drosophila melanogaster Immune Defense against Enterococcus faecalis

by Joanne R Chapman, Maureen A Dowell, Rosanna Chan and Robert L Unckless

Genes 2020, 11(2), 234; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11020234 - 22 Feb 2020

Cited by 11 | Viewed by 4063

Abstract

Dissecting the genetic basis of natural variation in disease response in hosts provides insights into the coevolutionary dynamics of host-pathogen interactions. Here, a genome-wide association study of Drosophila melanogaster survival after infection with the Gram-positive entomopathogenic bacterium Enterococcus faecalis is reported. There was considerable variation in defense against E. faecalis infection among inbred lines of the Drosophila Genetics Reference Panel. We identified single nucleotide polymorphisms associated with six genes with a significant (p < 10⁻⁰⁸, corresponding to a false discovery rate of 2.4%) association with survival, none of which were canonical immune genes. To validate the role of these genes in immune defense, their expression was knocked-down using RNAi and survival of infected hosts was followed, which confirmed a role for the genes krishah and S6k in immune defense. We further identified a putative role for the Bomanin gene BomBc1 (also known as IM23), in E. faecalis infection response. This study adds to the growing set of association studies for infection in Drosophila melanogaster and suggests that the genetic causes of variation in immune defense differ for different pathogens. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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14 pages, 1449 KiB

Open AccessArticle

Effect of Phenotype Selection on Genome Size Variation in Two Species of Diptera

by Carl E. Hjelmen, Jonathan J. Parrott, Satyam P. Srivastav, Alexander S. McGuane, Lisa L. Ellis, Andrew D. Stewart, J. Spencer Johnston and Aaron M. Tarone

Genes 2020, 11(2), 218; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11020218 - 19 Feb 2020

Cited by 8 | Viewed by 3365

Abstract

Genome size varies widely across organisms yet has not been found to be related to organismal complexity in eukaryotes. While there is no evidence for a relationship with complexity, there is evidence to suggest that other phenotypic characteristics, such as nucleus size and cell-cycle time, are associated with genome size, body size, and development rate. However, what is unknown is how the selection for divergent phenotypic traits may indirectly affect genome size. Drosophila melanogaster were selected for small and large body size for up to 220 generations, while Cochliomyia macellaria were selected for 32 generations for fast and slow development. Size in D. melanogaster significantly changed in terms of both cell-count and genome size in isolines, but only the cell-count changed in lines which were maintained at larger effective population sizes. Larger genome sizes only occurred in a subset of D. melanogaster isolines originated from flies selected for their large body size. Selection for development time did not change average genome size yet decreased the within-population variation in genome size with increasing generations of selection. This decrease in variation and convergence on a similar mean genome size was not in correspondence with phenotypic variation and suggests stabilizing selection on genome size in laboratory conditions. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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15 pages, 2659 KiB

Open AccessArticle

Constitutive and Plastic Gene Expression Variation Associated with Desiccation Resistance Differences in the Drosophila americana Species Group

by Jeremy S Davis and Leonie C Moyle

Genes 2020, 11(2), 146; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11020146 - 30 Jan 2020

Cited by 7 | Viewed by 2570

Abstract

Stress response mechanisms are ubiquitous and important for adaptation to heterogenous environments and could be based on constitutive or plastic responses to environmental stressors. Here we quantify constitutive and plastic gene expression differences under ambient and desiccation stress treatments, in males and females of three species of Drosophila known to differ in desiccation resistance. Drosophila novamexicana survives desiccation trials significantly longer than the two subspecies of Drosophila americana, consistent with its natural species range in the desert southwest USA. We found that desiccation stress reduces global expression differences between species—likely because many general stress response mechanisms are shared among species—but that all species showed plastic expression changes at hundreds of loci during desiccation. Nonetheless, D. novamexicana had the fewest genes with significant plastic expression changes, despite having the highest desiccation resistance. Of the genes that were significantly differentially expressed between species—either within each treatment (>200 loci), constitutively regardless of treatment (36 loci), or with different species-specific plasticity (26 loci)—GO analysis did not find significant enrichment of any major gene pathways or broader functions associated with desiccation stress. Taken together, these data indicate that if gene expression changes contribute to differential desiccation resistance between species, these differences are likely shaped by a relatively small set of influential genes rather than broad genome-wide differentiation in stress response mechanisms. Finally, among the set of genes with the greatest between-species plasticity, we identified an interesting set of immune-response genes with consistent but opposing reaction norms between sexes, whose potential functional role in sex-specific mechanisms of desiccation resistance remains to be determined. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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Review

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Behavioral Evolution of Drosophila: Unraveling the Circuit Basis

by Kosei Sato, Ryoya Tanaka, Yuki Ishikawa and Daisuke Yamamoto

Genes 2020, 11(2), 157; https://0-doi-org.brum.beds.ac.uk/10.3390/genes11020157 - 01 Feb 2020

Cited by 17 | Viewed by 5151

Abstract

Behavior is a readout of neural function. Therefore, any difference in behavior among different species is, in theory, an outcome of interspecies diversification in the structure and/or function of the nervous system. However, the neural diversity underlying the species-specificity in behavioral traits and its genetic basis have been poorly understood. In this article, we discuss potential neural substrates for species differences in the courtship pulse song frequency and mating partner choice in the Drosophila melanogaster subgroup. We also discuss possible neurogenetic mechanisms whereby a novel behavioral repertoire emerges based on the study of nuptial gift transfer, a trait unique to D. subobscura in the genus Drosophila. We found that the conserved central circuit composed primarily of fruitless-expressing neurons (the fru-circuit) serves for the execution of courtship behavior, whereas the sensory pathways impinging onto the fru-circuit or the motor pathways downstream of the fru-circuit are susceptible to changes associated with behavioral species differences. Full article

(This article belongs to the Special Issue Genetic Basis of Phenotypic Variation in Drosophila and Other Insects)

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