High-Resolution Quantitative Trait Locus Mapping Reveals Sign Epistasis Controlling Ovariole Number Between Two Drosophila Species

Orgogozo, Virginie; Broman, Karl W.; Stern, David L.

doi:10.1534/genetics.105.054098

Cited by 52 publications

(53 citation statements)

References 63 publications

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“…Further study of the genetic architecture of ovariole number in Drosophila spp. has revealed genotype-by-environment interaction (Starmer et al 1998;Bergland et al 2008) and several loci of large effect that interact epistatically (Wayne et al 2001;Richard et al 2005;Orgogozo et al 2006).…”

Section: Discussionmentioning

confidence: 99%

The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

et al. 2009

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Ovarioles are the functional unit of the female insect reproductive organs and the number of ovarioles per ovary strongly influences egg-laying rate and fecundity. Social evolution in the honeybee (Apis mellifera) has resulted in queens with 200-360 total ovarioles and workers with usually 20 or less. In addition, variation in ovariole number among workers relates to worker sensory tuning, foraging behavior, and the ability to lay unfertilized male-destined eggs. To study the genetic architecture of worker ovariole number, we performed a series of crosses between Africanized and European bees that differ in worker ovariole number. Unexpectedly, these crosses produced transgressive worker phenotypes with extreme ovariole numbers that were sensitive to the social environment. We used a new selective pooled DNA interval mapping approach with two Africanized backcrosses to identify quantitative trait loci (QTL) underlying the transgressive ovary phenotype. We identified one QTL on chromosome 11 and found some evidence for another QTL on chromosome 2. Both QTL regions contain plausible functional candidate genes. The ovariole number of foragers was correlated with the sugar concentration of collected nectar, supporting previous studies showing a link between worker physiology and foraging behavior. We discuss how the phenotype of extreme worker ovariole numbers and the underlying genetic factors we identified could be linked to the development of queen traits.T HE number of ovariole filaments per ovary is an important female reproductive character that affects fecundity across insect taxa (Richard et al. 2005;Makert et al. 2006). Social insect lineages have evolved a strong dimorphism in ovariole number between reproductive and nonreproductive castes. For example, while most families of bees consistently have 6 total ovarioles, and most species in the family Apidae have 8, the highly social species in the genus Apis (the honeybees) have queens that can have .360 total ovarioles and workers that often have ,10 (Winston 1987;Michener 2003). This queen-worker dimorphism is of primary importance because it translates into differential reproductive potential that defines the social roles of these female castes (Winston 1987) and classifies social species in general (Sherman et al. 1995). Furthermore, ovary size (i.e., ovariole number) is the most sensitive indicator of caste-specific development in honeybees (Dedej et al. 1998). The extreme increase in ovariole number for queen honeybees enables high egg-laying rates (.1500 per day) and is apparently a result of selection for increased colony reproduction (growth and fission by swarming) (Seeley 1997). Honeybee queens are thus highly specialized for egg laying, similar to queens of several other social insect taxa, such as army ants or higher termites (Hö lldobler and Wilson 1990). Honeybee workers in contrast, do not normally reproduce but perform all other essential activities including foraging for nectar, pollen, and water; caring for brood; and building, main...

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Section: Discussionmentioning

confidence: 99%

The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

et al. 2009

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“…Sign epistasis occurs when a single mutation has a beneficial fitness effect on one genetic background but a deleterious effect on another . There is rapidly accumulating empirical evidence to support the idea that the sign, as well as the magnitude, of a mutation's fitness effect can depend upon the genetic background (Lehming et al 1990;Orgogozo et al 2006;Weinreich et al 2006;Poelwijk et al 2007). To date, most of the evidence for sign epistasis comes from microbes, and it has been shown to be potentially important in shaping evolutionary trajectories that lead to the acquisition of drug resistance (Lehming et al 1990;Weinreich et al 2006;Poelwijk et al 2007).…”

Section: S Ewall Wright Argued In the 1930smentioning

confidence: 99%

“…To date, most of the evidence for sign epistasis comes from microbes, and it has been shown to be potentially important in shaping evolutionary trajectories that lead to the acquisition of drug resistance (Lehming et al 1990;Weinreich et al 2006;Poelwijk et al 2007). The application of quantitative trait loci methods has also demonstrated the importance of sign epistasis in eukaryotic systems (Orgogozo et al 2006) and technological advances will continue to further our understanding of the genetic control of fitness landscapes.…”

Section: S Ewall Wright Argued In the 1930smentioning

confidence: 99%

The Frequency of Fitness Peak Shifts Is Increased at Expanding Range Margins Due to Mutation Surfing

Burton

Travis

2008

Genetics

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Dynamic species' ranges, those that are either invasive or shifting in response to environmental change, are the focus of much recent interest in ecology, evolution, and genetics. Understanding how range expansions can shape evolutionary trajectories requires the consideration of nonneutral variability and genetic architecture, yet the majority of empirical and theoretical work to date has explored patterns of neutral variability. Here we use forward computer simulations of population growth, dispersal, and mutation to explore how range-shifting dynamics can influence evolution on rugged fitness landscapes. We employ a two-locus model, incorporating sign epistasis, and find that there is an increased likelihood of fitness peak shifts during a period of range expansion. Maladapted valley genotypes can accumulate at an expanding range front through a phenomenon called mutation surfing, which increases the likelihood that a mutation leading to a higher peak will occur. Our results indicate that most peak shifts occur close to the expanding front. We also demonstrate that periods of range shifting are especially important for peak shifting in species with narrow geographic distributions. Our results imply that trajectories on rugged fitness landscapes can be modified substantially when ranges are dynamic.

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“…Most of these genetic studies, however, concentrated on one or a few traits. Moreover, these earlier trait-specific studies could not distinguish between genetic changes that were a consequence of host specialization vs. those that directly contributed to the host specialization per se (Bono et al 2008;Matzkin 2008; but see Sucena and Stern 2000;Jones 2004;Orgogozo et al 2006;McBride 2007;McGregor et al 2007). …”

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confidence: 96%

Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila sechellia

2009

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Changes in host specialization contribute to the diversification of phytophagous insects. When shifting to a new host, insects evolve new physiological, morphological, and behavioral adaptations. Our understanding of the genetic changes responsible for these adaptations is limited. For instance, we do not know how often host shifts involve gain-of-function vs. loss-of-function alleles. Recent work suggests that some genes involved in odor recognition are lost in specialists. Here we show that genes involved in detoxification and metabolism, as well as those affecting olfaction, have reduced gene expression in Drosophila sechellia-a specialist on the fruit of Morinda citrifolia. We screened for genes that differ in expression between D. sechellia and its generalist sister species, D. simulans. We also screened for genes that are differentially expressed in D. sechellia when these flies chose their preferred host vs. when they were forced onto other food. D. sechellia increases expression of genes involved with oogenesis and fatty acid metabolism when on its host. The majority of differentially expressed genes, however, appear downregulated in D. sechellia. For several functionally related genes, this decrease in expression is associated with apparent loss-of-function alleles. For example, the D. sechellia allele of Odorant binding protein 56e (Obp56e) harbors a premature stop codon. We show that knockdown of Obp56e activity significantly reduces the avoidance response of D. melanogaster toward M. citrifolia. We argue that apparent loss-of-function alleles like Obp56e potentially contributed to the initial adaptation of D. sechellia to its host. Our results suggest that a subset of genes reduce or lose function as a consequence of host specialization, which may explain why, in general, specialist insects tend to shift to chemically similar hosts.

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High-Resolution Quantitative Trait Locus Mapping Reveals Sign Epistasis Controlling Ovariole Number Between Two Drosophila Species

Cited by 52 publications

References 63 publications

The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

The Genetic Basis of Transgressive Ovary Size in Honeybee Workers

The Frequency of Fitness Peak Shifts Is Increased at Expanding Range Margins Due to Mutation Surfing

Genetic Changes Accompanying the Evolution of Host Specialization in Drosophila sechellia

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