Publications by authors named "Adam K Chippindale"

26 Publications

  • Page 1 of 1

The microevolutionary response to male-limited X-chromosome evolution in Drosophila melanogaster reflects macroevolutionary patterns.

J Evol Biol 2020 06 5;33(6):738-750. Epub 2020 Apr 5.

Department of Environmental and Life Sciences, Karlstad University, Karlstad, Sweden.

Due to its hemizygous inheritance and role in sex determination, the X-chromosome is expected to play an important role in the evolution of sexual dimorphism and to be enriched for sexually antagonistic genetic variation. By forcing the X-chromosome to only be expressed in males over >40 generations, we changed the selection pressures on the X to become similar to those experienced by the Y. This releases the X from any constraints arising from selection in females and should lead to specialization for male fitness, which could occur either via direct effects of X-linked loci or trans-regulation of autosomal loci by the X. We found evidence of masculinization via up-regulation of male-benefit sexually antagonistic genes and down-regulation of X-linked female-benefit genes. Potential artefacts of the experimental evolution protocol are discussed and cannot be wholly discounted, leading to several caveats. Interestingly, we could detect evidence of microevolutionary changes consistent with previously documented macroevolutionary patterns, such as changes in expression consistent with previously established patterns of sexual dimorphism, an increase in the expression of metabolic genes related to mito-nuclear conflict and evidence that dosage compensation effects can be rapidly altered. These results confirm the importance of the X in the evolution of sexual dimorphism and as a source for sexually antagonistic genetic variation and demonstrate that experimental evolution can be a fruitful method for testing theories of sex chromosome evolution.
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http://dx.doi.org/10.1111/jeb.13618DOI Listing
June 2020

Experimental evolution of response to anoxia in : recovery of locomotion following CO or N exposure.

J Exp Biol 2019 07 25;222(Pt 14). Epub 2019 Jul 25.

Department of Biology, Queen's University, Kingston, ON, Canada, K7L 3N6

Many insects enter coma upon exposure to anoxia, a feature routinely exploited by experimentalists to handle them. But the genetic and physiological bases of anoxic coma induction and recovery are only partially understood, as are the long-term consequences for the animal's performance. We examined three populations of (designated B) that have been inadvertently under selection for rapid recovery from CO exposure for nearly 40 years (around 1000 generations) resulting from routine maintenance practices. We contrasted CO and N (presumed a less reactive gas) knockdown and recovery times of these B flies with six populations of common ancestry (A and C populations) that were not exposed to CO over the same period. We found that B populations showed faster and more consistent locomotor recovery than A or C populations after CO knockdown, a result also observed with N knockdown. A and C populations showed much higher variance in recovery time after CO exposure than after N exposure, suggesting gas-specific effects on pathways associated with locomotor recovery. Although these selection treatments result in considerable variation in life history attributes and body size, with the characteristic intermediacy of B populations, their superiority in resistance to gas exposure and locomotor recovery suggests that this is a direct consequence of prior repeated exposure to anoxia, broadly, and CO, specifically. Hence we describe a powerful new evolutionary model for the genetic and physiological investigation of anoxic coma in insects.
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http://dx.doi.org/10.1242/jeb.199521DOI Listing
July 2019

Direct benefits of choosing a high-fitness mate can offset the indirect costs associated with intralocus sexual conflict.

Evolution 2017 06 28;71(6):1710-1718. Epub 2017 Apr 28.

Department of Biology, Queen's University, Kingston, Ontario, K7L 3N6, Canada.

Intralocus sexual conflict generates a cost to mate choice: high-fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential "good genes" benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high-fitness males produced 11% more offspring compared to those mated to low-fitness males, and high-fitness females produced 34% more offspring than low-fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high-fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.
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http://dx.doi.org/10.1111/evo.13240DOI Listing
June 2017

Does kin selection moderate sexual conflict in Drosophila?

Proc Biol Sci 2015 Aug;282(1813):20151417

Department of Biology, Queen's University, Kingston, Ontario, Canada K7L 3N6.

Two recent studies provide provocative experimental findings about the potential influence of kin recognition and cooperation on the level of sexual conflict in Drosophila melanogaster. In both studies, male fruit flies apparently curbed their mate-harming behaviours in the presence of a few familiar or related males, suggesting some form of cooperation mediated by kin selection. In one study, the reduction in agonistic behaviour by brothers apparently rendered them vulnerable to dramatic loss of paternity share when competing with an unrelated male. If these results are robust and generalizable, fruit flies could be a major new focus for the experimental study of kin selection and social evolution. In our opinion, however, the restrictive conditions required for male cooperation to be adaptive in this species make it unlikely to evolve. We investigated these phenomena in two different populations of D. melanogaster using protocols very similar to those in the two previous studies. Our experiments show no evidence for a reduction in mate harm based upon either relatedness or familiarity between males, and no reduction in male reproductive success when two brothers are in the presence of an unfamiliar, unrelated, 'foreign' male. Thus, the reduction of sexual conflict owing to male cooperation does not appear to be a general feature of the species, at least under domestication, and these contrasting results call for further investigation: in new populations, in the field and in the laboratory populations in which these phenomena have been reported.
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http://dx.doi.org/10.1098/rspb.2015.1417DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4632634PMC
August 2015

Monitoring the developmental impact of copper and silver nanoparticle exposure in Drosophila and their microbiomes.

Sci Total Environ 2014 Jul 22;487:822-9. Epub 2014 Jan 22.

Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada; School of Environmental Studies, Queen's University, Kingston, Ontario K7L 3N6, Canada. Electronic address:

There is concern that waste waters containing manufactured metal nanoparticles (NPs) originating from consumer goods, will find their way into streams and larger water bodies. Aquatic invertebrates could be vulnerable to such pollution, and here we have used fruit flies, Drosophila melanogaster, as a model invertebrate, to test for the effect of NPs on fitness. Both copper NP and microparticle (MP)-containing medium slowed development, reduced adult longevity and decreased sperm competition. In contrast, ingestion of silver resulted in a significant reduction in developmental success only if the metal particles were nanosized. Ag NP-treatments resulted in reduced developmental success as assessed by larval and pupal survival as well as larval climbing ability, but there was no impact of silver on adult longevity and little effect on reproductive success. However, Cu NPs generally appeared to be no more toxic to this invertebrate model than the bulk counterpart. The impact of silver ingestion in larvae was further investigated by 454 pyrosequencing of the 16S rRNA genes of the midgut flora. There was a striking reduction in the diversity of the gut microbiota of Ag NP-treated larvae with a rise in the predominance of Lactobacillus brevis and a decrease in Acetobacter compared to control or Ag MP-treatment groups. Importantly, these experiments show that perturbation of the microbial assemblage within a metazoan model may contribute to Ag NP-mediated toxicity. These observations have implications for impact assessments of nanoparticles as emerging contaminants.
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http://dx.doi.org/10.1016/j.scitotenv.2013.12.129DOI Listing
July 2014

Mutation, condition, and the maintenance of extended lifespan in Drosophila.

Curr Biol 2013 Nov 7;23(22):2283-2287. Epub 2013 Nov 7.

Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada.

The evolutionary theory of aging predicts that longevity will decline via drift or age-specific tradeoffs when selection favors early life fitness. Many Drosophila melanogaster populations continually terminated at young adult ages retain surprisingly long postselection lifespans. We compiled three decades of longevity data from the Ives population, demonstrating that postselective longevity was both substantial (30 days) and temporally stable over this period. Recently, alleles with positive pleiotropic effects between adjacent ages, particularly those affecting overall condition, have been integrated into the theory and may explain the extended longevity observed. We experimentally tested this hypothesis by isolating 20 hemiclones from Ives and allowing spontaneous mutations to accumulate (MA) for 35 generations. Fitness and longevity were positively genetically correlated in control females, and both traits declined due to MA. Crucially, MA induced a strong positive genetic correlation between the traits in both sexes, implying that mutations with early-life impacts also reduce late-life survival. Our results suggest that extended postreproductive longevity is actively maintained by selection for early-life fitness via positive pleiotropy and is not a merely a byproduct of exhaustion of genetic variation or weak drift. Thus mutation-selection balance for early fitness may govern variance in longevity in this system: a balance struck remarkably long after selection for continued survival ceases.
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http://dx.doi.org/10.1016/j.cub.2013.09.049DOI Listing
November 2013

Evolution: sperm, cryptic choice, and the origin of species.

Curr Biol 2013 Oct;23(19):R885-7

Department of Biology, Queen's University, Kingston K7L 3N6, Canada. Electronic address:

In two fruit fly species, in vivo observations of competing sperm reveal how differences in sperm size, female behavior and reproductive architecture promote retention of same-species sperm. Sexual selection continues after mating and may play an important role in speciation.
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http://dx.doi.org/10.1016/j.cub.2013.08.024DOI Listing
October 2013

Epigenetics and sex-specific fitness: an experimental test using male-limited evolution in Drosophila melanogaster.

PLoS One 2013 29;8(7):e70493. Epub 2013 Jul 29.

Department of Biology, Section for Evolutionary Ecology, Lund University, Lund, Sweden.

When males and females have different fitness optima for the same trait but share loci, intralocus sexual conflict is likely to occur. Epigenetic mechanisms such as genomic imprinting (in which expression is altered according to parent-of-origin) and sex-specific maternal effects have been suggested as ways by which this conflict can be resolved. However these ideas have not yet been empirically tested. We designed an experimental evolution protocol in Drosophila melanogaster that enabled us to look for epigenetic effects on the X-chromosome-a hotspot for sexually antagonistic loci. We used special compound-X females to enforce father-to-son transmission of the X-chromosome for many generations, and compared fitness and gene expression levels between Control males, males with a Control X-chromosome that had undergone one generation of father-son transmission, and males with an X-chromosome that had undergone many generations of father-son transmission. Fitness differences were dramatic, with experimentally-evolved males approximately 20% greater than controls, and with males inheriting a non-evolved X from their father about 20% lower than controls. These data are consistent with both strong intralocus sexual conflict and misimprinting of the X-chromosome under paternal inheritance. However, expression differences suggested that reduced fitness under paternal X inheritance was largely due to deleterious maternal effects. Our data confirm the sexually-antagonistic nature of Drosophila's X-chromosome and suggest that the response to male-limited X-chromosome evolution entails compensatory evolution for maternal effects, and perhaps modification of other epigenetic effects via coevolution of the sex chromosomes.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0070493PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3726629PMC
August 2014

A cryptic rock-paper-scissors game between Drosophila males.

Mol Ecol 2013 Mar;22(5):1190-2

Department of Biology, Queen's University, Kingston, ON, Canada.

Explaining the maintenance of genetic variation in characters associated with Darwinian fitness is a preoccupation of evolutionary biologists. Spatial or temporal variation in the environment can certainly promote polymorphism, yet even populations of 'model organisms', like fruit flies, kept on invariant protocols for hundreds of generations in the laboratory often show fitness variation that exceeds what would be expected from the input of new mutations alone. Such observations suggest either complexities of selection or of genetic architecture, and offer a powerful tool for the study of mechanisms that promote stable polymorphism. In this issue of Molecular Ecology, Zhang et al. (2013) report examples of nontransitivity in the outcome of postcopulatory sexual selection in the fruit fly, Drosophila, that follow the rules of the popular stalemate-breaking game roshambo - or rock, paper, scissors (RPS). The important feature of RPS is that while each strategy beats one other, it in turn is beaten by the third. Using chromosome extraction lines, the authors confirm earlier findings that the outcome of postcopulatory sexual selection via sperm competition for a male depends, in part, upon the competitor male's genotype. But taking it one step further, they demonstrate the nontransitivities between males required for circular RPS cycles in sperm competition between males, and are able to identify at least four associated loci. Because the postmating phenotype involves hundreds of potentially interacting peptides and receptors, this is an important step to understanding the persistence of variation in a critical component of male fitness.
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http://dx.doi.org/10.1111/mec.12208DOI Listing
March 2013

Male-limited evolution suggests no extant intralocus sexual conflict over the sexually dimorphic cuticular hydrocarbons of Drosophila melanogaster.

J Genet 2011 Dec;90(3):443-52

Department of Biology, Queen's University, 116 Barrie Street, Kingston, ON K7L3N6, Canada.

Sexually dimorphic traits are likely to have evolved through sexually antagonistic selection. However, recent empirical data suggest that intralocus sexual conflict often persists, even when traits have diverged between males and females. This implies that evolved dimorphism is often incomplete in resolving intralocus conflict, providing a mechanism for the maintenance of genetic variance in fitness-related traits. We used experimental evolution in Drosophila melanogaster to directly test for ongoing conflict over a suite of sexually dimorphic cuticular hydrocarbons (CHCs) that are likely targets of sex-specific selection. Using a set of experimental populations in which the transmission of genetic material had been restricted to males for 82 generations, we show that CHCs did not evolve, providing experimental evidence for the absence of current intralocus sexual conflict over these traits. The absence of ongoing conflict could indicate that CHCs have never been the target of sexually antagonistic selection, although this would require the existing dimorphism to have evolved via completely sexlinked mutations or as a result of former, but now absent, pleiotropic effects of the underlying loci on another trait under sexually antagonistic selection. An alternative interpretation, and which we believe to be more likely, is that the extensive CHC sexual dimorphism is the result of past intralocus sexual conflict that has been fully resolved, implying that these traits have evolved genetic independence between the sexes and that genetic variation in them is therefore maintained by alternative mechanisms. This latter interpretation is consistent with the known roles of CHCs in sexual communication in this species and with previous studies suggesting the genetic independence of CHCs between males and females. Nevertheless, direct estimates of sexually antagonistic selection will be important to fully resolve these alternatives.
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http://dx.doi.org/10.1007/s12041-011-0109-3DOI Listing
December 2011

Susceptibility of the male fitness phenotype to spontaneous mutation.

Biol Lett 2012 Jun 16;8(3):426-9. Epub 2011 Nov 16.

Department of Biology, Queen's University, Kingston, Ontario, Canada.

Adult reproductive success can account for a large fraction of male fitness, however, we know relatively little about the susceptibility of reproductive traits to mutation-accumulation (MA). Estimates of the mutational rate of decline for adult fitness and its components are controversial in Drosophila melanogaster, and post-copulatory performance has not been examined. We therefore separately measured the consequences of MA for total male reproductive success and its major pre-copulatory and post-copulatory components: mating success and sperm competitive success. We also measured juvenile viability, an important fitness component that has been well studied in MA experiments. MA had strongly deleterious effects on both male viability and adult fitness, but the latter declined at a much greater rate. Mutational pressure on total fitness is thus much greater than would be predicted by viability alone. We also noted a significant and positive correlation between all adult traits and viability in the MA lines, suggesting pleiotropy of mutational effect as required by 'good genes' models of sexual selection.
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http://dx.doi.org/10.1098/rsbl.2011.0977DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3367732PMC
June 2012

About PAR: the distinct evolutionary dynamics of the pseudoautosomal region.

Trends Genet 2011 Sep;27(9):358-67

Department of Zoology, 6270 University Boulevard, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.

Sex chromosomes differ from other chromosomes in the striking divergence they often show in size, structure, and gene content. Not only do they possess genes controlling sex determination that are restricted to either the X or Y (or Z or W) chromosomes, but in many taxa they also include recombining regions. In these 'pseudoautosomal regions' (PARs), sequence homology is maintained by meiotic pairing and exchange in the heterogametic sex. PARs are unique genomic regions, exhibiting some features of autosomes, but they are also influenced by their partial sex linkage. Here we review the distribution and structure of PARs among animals and plants, the theoretical predictions concerning their evolutionary dynamics, the reasons for their persistence, and the diversity and content of genes that reside within them. It is now clear that the evolution of the PAR differs in important ways from that of genes in either the non-recombining regions of sex chromosomes or the autosomes.
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http://dx.doi.org/10.1016/j.tig.2011.05.001DOI Listing
September 2011

Experimental mutation-accumulation on the X chromosome of Drosophila melanogaster reveals stronger selection on males than females.

BMC Evol Biol 2011 Jun 6;11:156. Epub 2011 Jun 6.

Department of Biology, Queen's University, Kingston, ON, Canada.

Background: Sex differences in the magnitude or direction of mutational effect may be important to a variety of population processes, shaping the mutation load and affecting the cost of sex itself. These differences are expected to be greatest after sexual maturity. Mutation-accumulation (MA) experiments provide the most direct way to examine the consequences of new mutations, but most studies have focused on juvenile viability without regard to sex, and on autosomes rather than sex chromosomes; both adult fitness and X-linkage have been little studied. We therefore investigated the effects of 50 generations of X-chromosome mutation accumulation on the fitness of males and females derived from an outbred population of Drosophila melanogaster.

Results: Fitness declined rapidly in both sexes as a result of MA, but adult males showed markedly greater fitness loss relative to their controls compared to females expressing identical genotypes, even when females were made homozygous for the X. We estimate that these mutations are partially additive (h ~ 0.3) in females. In addition, the majority of new mutations appear to harm both males and females.

Conclusions: Our data helps fill a gap in our understanding of the consequences of sexual selection for genetic load, and suggests that stronger selection on males may indeed purge deleterious mutations affecting female fitness.
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http://dx.doi.org/10.1186/1471-2148-11-156DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3134001PMC
June 2011

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance.

J Genet 2008 Dec;87(4):383-94

Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada.

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males' fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.
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http://dx.doi.org/10.1007/s12041-008-0061-zDOI Listing
December 2008

Reproductive behaviour evolves rapidly when intralocus sexual conflict is removed.

PLoS One 2008 May 14;3(5):e2187. Epub 2008 May 14.

Department of Biology, Queen's University, Kingston, Ontario, Canada.

Background: Intralocus sexual conflict can inhibit the evolution of each sex towards its own fitness optimum. In a previous study, we confirmed this prediction through the experimental removal of female selection pressures in Drosophila melanogaster, achieved by limiting the expression of all major chromosomes to males. Compared to the control populations (C(1-4)) where the genomes are exposed to selection in both sexes, the populations with male-limited genomes (ML(1-4)) showed rapid increases in male fitness, whereas the fitness of females expressing ML-evolved chromosomes decreased.

Methodology/principal Findings: Here we examine the behavioural phenotype underlying this sexual antagonism. We show that males expressing the ML genomes have a reduced courtship level but acquire the same number of matings. On the other hand, our data suggest that females expressing the ML genomes had reduced attractiveness, stimulating a lower rate of courtship from males. Moreover, females expressing ML genomes tend to display reduced yeast-feeding behaviour, which is probably linked to the reduction of their fecundity.

Conclusion/significance: These results suggest that reproductive behaviour is shaped by opposing selection on males and females, and that loci influencing attractiveness and foraging were polymorphic for alleles with sexually antagonistic expression patterns prior to ML selection. Hence, intralocus sexual conflict appears to play a role in the evolution of a wide range of fitness-related traits and may be a powerful mechanism for the maintenance of genetic variation in fitness.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0002187PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2367451PMC
May 2008

Intralocus sexual conflict diminishes the benefits of sexual selection.

PLoS Biol 2006 Nov;4(11):e356

Department of Biology, Queen's University, Kingston, Ontario, Canada.

Evolution based on the benefits of acquiring "good genes" in sexual selection is only plausible with the reliable transmission of genetic quality from one generation to the next. Accumulating evidence suggests that sexually antagonistic (SA) genes with opposite effects on Darwinian fitness when expressed in the two different sexes may be common in animals and plants. These SA genes should weaken the potential indirect genetic benefits of sexual selection by reducing the fitness of opposite-sex progeny from high-fitness parents. Here we use hemiclonal analysis in the fruit fly, Drosophila melanogaster, to directly measure the inheritance of fitness across generations, over the entire genome. We show that any potential genetic benefits of sexual selection in this system are not merely weakened, but completely reversed over one generation because high-fitness males produce low-fitness daughters and high-fitness mothers produce low-fitness sons. Moreover, male fitness was not inherited by sons, consistent with both theory and recent evidence connecting this form of SA variation with the X chromosome. This inheritance pattern may help to explain how genetic variation for fitness is sustained despite strong sexual selection, and why the ZW sex chromosome system found in birds and butterflies appears to foster the evolution of extreme secondary sexual characters in males.
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http://dx.doi.org/10.1371/journal.pbio.0040356DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1618422PMC
November 2006

Quantifying the gender load: can population crosses reveal interlocus sexual conflict?

Philos Trans R Soc Lond B Biol Sci 2006 Feb;361(1466):363-74

Department of Biology, Queen's University, Kingston, Ontario K7L 3N6, Canada.

Six sister populations of Drosophila melanogaster kept under identical environmental conditions for greater than 600 generations were reciprocally crossed to investigate the incidence of population divergence in allopatry. Population crosses directly influenced fitness, mating frequency, and sperm competition patterns. Changes in both female remating rate and the outcome of male sperm competition (P1, P2) in response to foreign males were consistent with intersexual coevolution. Moreover, seven of the 30 crosses between foreign mates resulted in significant reductions in female fitness, whereas two resulted in significant increases, compared to local matings. This tendency for foreign males to reduce female fitness may be interpreted as evidence for either sexually antagonistic coevolution or the disruption of mutualistic interactions. However, instances in which female fitness improved via cohabitation with foreign males may better reveal sexual conflict, signalling release from the cost of interacting with locally adapted males. By this metric, female reproduction in D. melanogaster is strongly constrained by local adaptation by males, a situation that would promote antagonistic coevolution between the sexes. We conclude that sexual selection can promote population differentiation in allopatry and that sexual conflict is likely to have played a role in population differentiation in this study system.
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http://dx.doi.org/10.1098/rstb.2005.1786DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1569607PMC
February 2006

The devil in the details of life-history evolution: instability and reversal of genetic correlations during selection on Drosophila development.

J Genet 2003 Dec;82(3):133-45

Department of Biology, Queen's University, Kingston, ON K7L 3N6, Canada.

The evolutionary relationships between three major components of Darwinian fitness, development rate, growth rate and preadult survival, were estimated using a comparison of 55 distinct populations of Drosophila melanogaster variously selected for age-specific fertility, environmental-stress tolerance and accelerated development. Development rate displayed a strong net negative evolutionary correlation with weight at eclosion across all selection treatments, consistent with the existence of a size-versus-time tradeoff between these characters. However, within the data set, the magnitude of the evolutionary correlation depended upon the particular selection treatments contrasted. A previously proposed tradeoff between preadult viability and growth rate was apparent only under weak selection for juvenile fitness components. Direct selection for rapid development led to sharp reductions in both growth rates and viability. These data add to the mounting results from experimental evolution that illustrate the sensitivity of evolutionary correlations to (i) genotype-by-environment (G x E) interaction, (ii) complex functional-trait interactions, and (iii) character definition. Instability, disappearance and reversal of patterns of genetic covariation often occur over short evolutionary time frames and as the direct product of selection, rather than some stochastic process. We suggest that the functional architecture of fitness is a rapidly evolving matrix with reticulate properties, a matrix that we understand only poorly.
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http://dx.doi.org/10.1007/BF02715814DOI Listing
December 2003

Breakdown in correlations during laboratory evolution. I. Comparative analyses of Drosophila populations.

Evolution 2003 Mar;57(3):527-35

Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697, USA.

We provide evidence from comparisons of populations of Drosophila that evolutionary correlations between longevity and stress resistance break down over the course of laboratory evolution. Using 15 distinct evolutionary regimes, we created 75 populations that were differentiated for early fecundity, longevity, starvation resistance, desiccation resistance, and developmental time. In earlier experiments, selection for postponed aging produced increases in stress resistance, whereas selection for increased stress resistance produced increases in longevity. Direct estimates of correlations also indicated an antagonistic relationship between early fecundity on one hand and longevity or stress resistance on the other. Laboratory evolution of extreme values of stress resistance, however, led to a breakdown in these evolutionary relationships. There was no evidence that these significant changes in correlation resulted from genotype-by-environment interactions or inbreeding. These findings suggest that correlations between functional characters are not necessarily durable features of a species, and that short-term evolutionary responses cannot be extrapolated reliably to longer-term evolutionary patterns.
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http://dx.doi.org/10.1111/j.0014-3820.2003.tb01544.xDOI Listing
March 2003

The evolution of hybrid infertility: perpetual coevolution between gender-specific and sexually antagonistic genes.

Genetica 2002 Nov;116(2-3):179-88

Department of Ecology, Evolution and Marine Biology, University of California, Santa Barbara, CA, USA.

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a 'gender-load' in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.
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November 2002

The X chromosome is a hot spot for sexually antagonistic fitness variation.

Proc Biol Sci 2002 Mar;269(1490):499-505

Department of Ecology, Evolution and Marine Biology, University of California at Santa Barbara, Santa Barbara, CA 93106-9610, USA.

Sexually antagonistic alleles are selected discordantly between the sexes. Experimental evidence indicates that sexually antagonistic fitness variation is abundant in the genome of Drosophila melanogaster. Theory predicts that the X chromosome will be enriched with this type of variation. To test this prediction in D. melanogaster, we sampled, and cytogenetically cloned, 20 X chromosomes and compared their fitness variation to genome-wide levels. At the juvenile stage, in which gender roles are most similar, the X chromosome made no detectable contribution to genome-wide fitness variation. At the adult stage, in which gender roles diverge, the X chromosome was estimated to harbour 45% of the genome-wide fitness variation and 97% of the genome-wide sexually antagonistic variation. This genomic structure has important implications for the process of sexual selection because X-linked sexually antagonistic variation contributes to negative intersexual heritability for fitness, i.e. high-fitness males (females) produce, on average, low-fitness daughters (sons).
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http://dx.doi.org/10.1098/rspb.2001.1863DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1690921PMC
March 2002

RESOURCE ACQUISITION AND THE EVOLUTION OF STRESS RESISTANCE IN DROSOPHILA MELANOGASTER.

Evolution 1998 Oct;52(5):1342-1352

Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92697-2525.

Resistance to environmental stress is one of the most important forces molding the distribution and abundance of species. We investigated the evolution of desiccation stress resistance using 20 outbred Drosophila melanogaster populations directly selected in the laboratory for adult desiccation resistance (D), postponed senescence (O), and their respective controls (C and B). Both aging and desiccation selection increased desiccation resistance relative to their controls, creating a spectrum of desiccation resistance levels across selection treatments. We employed an integrative approach, merging data on the life histories of these populations with a detailed physiology of water balance. The physiological basis of desiccation resistance may be mechanisms enhancing either resource conservation or resource acquisition and allocation. Desiccation-resistant populations had increased water and carbohydrate stores, and showed age-specific patterns of desiccation resistance consistent with the resource accumulation mechanism. A significant proportion of the resources relevant to resistance of the stress were accumulated in the larval stage. Males and females of desiccation-selected lines exhibited distinctly different patterns of desiccation resistance and resource acquisition, in a manner suggesting intersexual antagonism in the evolution of stress resistance. Preadult viability of stress-selected populations was lower than that of controls, and development was slowed. Our results suggest that there is a cost to preadult resource acquisition, pointing out a complex trade-off architecture involving characters distributed across distinct life-cycle stages.
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http://dx.doi.org/10.1111/j.1558-5646.1998.tb02016.xDOI Listing
October 1998

EXPERIMENTAL EVOLUTION OF ACCELERATED DEVELOPMENT IN DROSOPHILA. 1. DEVELOPMENTAL SPEED AND LARVAL SURVIVAL.

Evolution 1997 Oct;51(5):1536-1551

Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92717-2525.

Developmental time is a trait of great relevance to fitness in all organisms. In holometabolous species that occupy ephemeral habitat, like Drosophila melanogaster, the impact of developmental time upon fitness is further exaggerated. We explored the trade-offs surrounding developmental time by selecting 10 independent populations from two distantly related selection treatments (CB and CO ) for faster development. After 125 generations, the resulting accelerated populations (ACB and ACO ) displayed net selection responses for development time of -33.4 hours (or 15%) for ACB and -38.6 hours (or 17%) for ACO. Since most of the change in egg-to-adult developmental time was accounted for by changes in larval duration, the "accelerated" larvae were estimated to develop 25-30% faster than their control/ancestor populations. The responses of ACB and ACO lines were remarkably parallel, despite being founded from populations evolved independently for more than 300 generations. On average, these "A" populations developed from egg to adult in less than eight days and produced fertile eggs less than 24 hours after emerging. Accelerated populations showed no change in larval feeding rate, but a reduction in pupation height, the latter being a trait relating to larval energetic expenditure in wandering prior to pupation. This experiment demonstrates the existence of a negative evolutionary correlation between preadult developmental time and viability, as accelerated populations experienced a severe cost in preadult survivorship. In the final assay generation, viability of accelerated treatments had declined by more than 10%, on average. A diallel cross demonstrated that the loss of viability in the ACO lines was not due to inbreeding depression. These results suggest the existence of a rapid development syndrome, in which the fitness benefits of fast development are balanced by fitness costs resulting from reduced preadult survivorship, marginal larval storage of metabolites, and reduced adult size.
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http://dx.doi.org/10.1111/j.1558-5646.1997.tb01477.xDOI Listing
October 1997

COMPLEX TRADE-OFFS AND THE EVOLUTION OF STARVATION RESISTANCE IN DROSOPHILA MELANOGASTER.

Evolution 1996 Apr;50(2):753-766

Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92717.

The measurement of trade-offs may be complicated when selection exploits multiple avenues of adaptation or multiple life-cycle stages. We surveyed 10 populations of Drosophila melanogaster selected for increased resistance to starvation for 60 generations, their paired controls, and their mutual ancestors (a total of 30 outbred populations) for evidence of physiological and life-history trade-offs that span life-cycle stages. The directly selected lines showed an impressive response to starvation selection, with mature adult females resisting starvation death 4-6 times longer than unselected controls or ancestors-up to a maximum of almost 20 days. Starvation-selected flies are already 80% more resistant to starvation death than their controls immediately upon eclosion, suggesting that a significant portion of their selection response was owing to preadult growth and acquisition of metabolites relevant to the stress. These same lines exhibited significantly longer development and lower viability in the larval and pupal stages. Weight and lipid measurements on one of the starvation-selected treatments (SB ), its control populations (CB ), and their ancestor populations (B ) revealed three important findings. First, starvation resistance and lipid content were linearly correlated; second, larval lipid acquisition played a major role in the evolution of adult starvation resistance; finally, increased larval growth rate and lipid acquisition had a fitness cost exacted in reduced viability and slower development. This study implicates multiple life-cycle stages in the response to selection for the stress resistance of only one stage. Our starvation-selected populations illustrate a case that may be common in nature. Patterns of genetic correlation may prove misleading unless multiple pleiotropic interconnections are resolved.
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http://dx.doi.org/10.1111/j.1558-5646.1996.tb03885.xDOI Listing
April 1996

THE EVOLUTION OF DEVELOPMENT IN DROSOPHILA MELANOGASTER SELECTED FOR POSTPONED SENESCENCE.

Evolution 1994 Dec;48(6):1880-1899

Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92717.

The role of development in the evolution of postponed senescence is poorly understood despite the existence of a major gerontological theory connecting developmental rate to aging. We investigate the role of developmental rate in the laboratory evolution of aging using 24 distinct populations of Drosophila melanogaster. We have found a significant difference between the larval developmental rates of our Drosophila stocks selected for early (B) and late-life (O) fertility. This larval developmental time difference of approximately 12% (O > B) has been stable for at least 5 yr, occurs under a wide variety of rearing conditions, responds to reverse selection, and is shown for two other O-like selection treatments. Emerging adults from lines with different larval developmental rates show no significant differences in weight at emergence, thorax length, or starvation resistance. Long-developing lines (O, CO, and CB) have greater survivorship from egg to pupa and from pupa to adult, with and without strong larval competition. Crosses between slower developing populations, and a variety of other lines of evidence, indicate that neither mutation accumulation nor inbreeding depression are responsible for the extended development of our late-reproduced selection treatments. These results stand in striking contrast to other recent studies. We argue that inbreeding depression and inadvertent direct selection in other laboratories' culture regimes explain their results. We demonstrate antagonistic pleiotropy between developmental rate and preadult viability. The absence of any correlation between longevity and developmental time in our stocks refutes the developmental theory of aging.
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http://dx.doi.org/10.1111/j.1558-5646.1994.tb02221.xDOI Listing
December 1994

LONG-TERM LABORATORY EVOLUTION OF A GENETIC LIFE-HISTORY TRADE-OFF IN DROSOPHILA MELANOGASTER. 1. THE ROLE OF GENOTYPE-BY-ENVIRONMENT INTERACTION.

Evolution 1994 Aug;48(4):1244-1257

Department of Ecology and Evolutionary Biology, University of California, Irvine, California, 92717.

Trade-offs among life-history traits are often thought to constrain the evolution of populations. Here we report the disappearance of a trade-off between early fecundity on the one hand, and late-life fecundity, starvation resistance, and longevity on the other, over 10 yr of laboratory selection for late-life reproduction. Whereas the selected populations showed an initial depression in early-life fecundity, they later converged upon the controls and then surpassed them. The evolutionary loss of the trade-off among life-history traits is considered attributable to the following factors: (1) the existence of differences in the culture regimes of the short- and long-generation populations other than the demographic differences deliberately imposed; (2) adaptation of one or both of these sets of populations to the unique aspects of their culture regimes; (3) the existence of an among-environment trade-off in the expression of early fecundity in the two culture regimes, as reflected in assays that mimic those regimes. The trade-off between early and late-life reproductive success, as manifest among divergently selected populations, is apparent or not depending on the assay environment. This demonstration that strong genotype-by-environment interactions can obscure a fundamental trade-off points to the importance of controlling all aspects of the culture regime of experimental populations and the difficulty of doing so even in the laboratory.
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http://dx.doi.org/10.1111/j.1558-5646.1994.tb05309.xDOI Listing
August 1994
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