| 1. |
- Brand, Jack A., et al.
(author)
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Temperature change exerts sex-specific effects on behavioural variation
- 2023
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In: Proceedings of the Royal Society of London. Biological Sciences. - 0962-8452 .- 1471-2954. ; 290:2002
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Journal article (peer-reviewed)abstract
- Temperature is a key factor mediating organismal fitness and has important consequences for species' ecology. While the mean effects of temperature on behaviour have been well-documented in ectotherms, how temperature alters behavioural variation among and within individuals, and whether this differs between the sexes, remains unclear. Such effects likely have ecological and evolutionary consequences, given that selection acts at the individual level. We investigated the effect of temperature on individual-level behavioural variation and metabolism in adult male and female Drosophila melanogaster (n = 129), by taking repeated measures of locomotor activity and metabolic rate at both a standard temperature (25°C) and a high temperature (28°C). Males were moderately more responsive in their mean activity levels to temperature change when compared to females. However, this was not true for either standard or active metabolic rate, where no sex differences in thermal metabolic plasticity were found. Furthermore, higher temperatures increased both among- and within-individual variation in male, but not female, locomotor activity. Given that behavioural variation can be critical to population persistence, we suggest that future studies test whether sex differences in the amount of behavioural variation expressed in response to temperature change may result in sex-specific vulnerabilities to a warming climate.
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| 2. |
- Yee, Winston K. W., et al.
(author)
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Intergenomic interactions between mitochondrial and Y-linked genes shape male mating patterns and fertility in Drosophila melanogaster
- 2015
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In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 69:11, s. 2876-2890
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Journal article (peer-reviewed)abstract
- Under maternal inheritance, mitochondrial genomes are prone to accumulate mutations that exhibit male-biased effects. Such mutations should, however, place selection on the nuclear genome for modifier adaptations that mitigate mitochondrial-incurred male harm. One gene region that might harbor such modifiers is the Y-chromosome, given the abundance of Y-linked variation for male fertility, and because Y-linked modifiers would not exert antagonistic effects in females because they would be found only in males. Recent studies in Drosophila revealed a set of nuclear genes whose expression is sensitive to allelic variation among mtDNA-and Y-haplotypes, suggesting these genes might be entwined in evolutionary conflict between mtDNA and Y. Here, we test whether genetic variation across mtDNA and Y haplotypes, sourced from three disjunct populations, interacts to affect male mating patterns and fertility across 10 days of early life in D. melanogaster. We also investigate whether coevolved mito-Y combinations outperform their evolutionarily novel counterparts, as predicted if the interacting Y-linked variance is comprised of modifier adaptations. Although we found no evidence that coevolved mito-Y combinations outperformed their novel counterparts, interactions between mtDNA and Y-chromosomes affected male mating patterns. These interactions were dependent on male age; thus male reproductive success was shaped by G x G x E interactions.
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| 3. |
- Arnqvist, Göran, et al.
(author)
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Genetic architecture of metabolic rate : environment specific epistasis between mitochondrial and nuclear genes in an insect
- 2010
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In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 64:12, s. 3354-3363
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Journal article (peer-reviewed)abstract
- The extent to which mitochondrial DNA (mtDNA) variation is involved in adaptive evolutionary change is currently being reevaluated. In particular, emerging evidence suggests that mtDNA genes coevolve with the nuclear genes with which they interact to form the energy producing enzyme complexes in the mitochondria. This suggests that intergenomic epistasis between mitochondrial and nuclear genes may affect whole-organism metabolic phenotypes. Here, we use crossed combinations of mitochondrial and nuclear lineages of the seed beetle Callosobruchus maculatus and assay metabolic rate under two different temperature regimes. Metabolic rate was affected by an interaction between the mitochondrial and nuclear lineages and the temperature regime. Sequence data suggests that mitochondrial genetic variation has a role in determining the outcome of this interaction. Our genetic dissection of metabolic rate reveals a high level of complexity, encompassing genetic interactions over two genomes, and genotype x genotype x environment interactions. The evolutionary implications of these results are twofold. First, because metabolic rate is at the root of life histories, our results provide insights into the complexity of life-history evolution in general, and thermal adaptation in particular. Second, our results suggest a mechanism that could contribute to the maintenance of nonneutral mtDNA polymorphism.
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| 4. |
- Camus, M. Florencia, et al.
(author)
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Single Nucleotides in the mtDNA Sequence Modify Mitochondrial Molecular Function and Are Associated with Sex-Specific Effects on Fertility and Aging
- 2015
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In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 25:20, s. 2717-2722
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Journal article (peer-reviewed)abstract
- Mitochondria underpin energy conversion in eukaryotes. Their small genomes have been the subject of increasing attention, and there is evidence that mitochondrial genetic variation can affect evolutionary trajectories and shape the expression of life-history traits considered to be key human health indicators [1, 2]. However, it is not understood how genetic variation across a diminutive genome, which in most species harbors only about a dozen protein-coding genes, can exert broad-scale effects on the organisnnal phenotype [2, 3]. Such effects are particularly puzzling given that the mitochondrial genes involved are under strong evolutionary constraint and that mitochondrial gene expression is highly conserved across diverse taxa [4]. We used replicated genetic lines in the fruit fly, Drosophila melanogaster, each characterized by a distinct and naturally occurring mitochondrial haplotype placed alongside an isogenic nuclear background. We demonstrate that sequence variation within the mitochondria! DNA (mtDNA) affects both the copy number of mitochondrial genomes and patterns of gene expression across key mitochondrial protein-coding genes. In several cases, haplotype-mediated patterns of gene expression were gene-specific, even for genes from within the same transcriptional units. This invokes post-transcriptional processing of RNA in the regulation of mitochondrial genetic effects on organismal phenotypes. Notably, the haplotype-mediated effects on gene expression could be traced backward to the level of individual nucleotides and forward to sex-specific effects on fertility and longevity. Our study thus elucidates how small-scale sequence changes in the mitochondrial genome can achieve broad-scale regulation of health-related phenotypes and even contribute to sex-related differences in longevity.
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| 5. |
- Dowling, Damian K., et al.
(author)
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A comparison of nuclear and cytoplasmic genetic effects on sperm competitiveness and female remating in a seed beetle
- 2007
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In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 20:6, s. 2113-2125
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Journal article (peer-reviewed)abstract
- It is widely assumed that male sperm competitiveness evolves adaptively. However, recent studies have found a cytoplasmic genetic component to phenotypic variation in some sperm traits presumed important in sperm competition. As cytoplasmic genes are maternally transmitted, they cannot respond to selection on sperm and this constraint may affect the scope in which sperm competitiveness can evolve adaptively. We examined nuclear and cytoplasmic genetic contributions to sperm competitiveness, using populations of Callosobruchus maculatus carrying orthogonal combinations of nuclear and cytoplasmic lineages. Our design also enabled us to examine genetic contributions to female remating. We found that sperm competitiveness and remating are primarily encoded by nuclear genes. In particular, a male's sperm competitiveness phenotype was contingent on an interaction between the competing male genotypes. Furthermore, cytoplasmic effects were detected on remating but not sperm competitiveness, suggesting that cytoplasmic genes do not generally play a profound evolutionary role in sperm competition.
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| 6. |
- Dowling, Damian K., et al.
(author)
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Cytonuclear Interactions and the Economics of Mating in Seed Beetles
- 2010
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In: American Naturalist. - : University of Chicago Press. - 0003-0147 .- 1537-5323. ; 176:2, s. 131-140
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Journal article (peer-reviewed)abstract
- Recent studies have uncovered an abundance of non-neutral cytoplasmic genetic variation within species, which suggests that we should no longer consider the cytoplasm an idle intermediary of evolutionary change. Nonneutrality of cytoplasmic genomes is particularly intriguing, given that these genomes are maternally transmitted. This means that the fate of any given cytoplasmic genetic mutation is directly tied to its performance when expressed in females. For this reason, it has been hypothesized that cytoplasmic genes will coevolve via a sexually antagonistic arms race with the biparentally transmitted nuclear genes with which they interact. We assess this prediction, examining the intergenomic contributions to the costs and benefits of mating in Callosobruchus maculatus females subjected to a mating treatment with three classes (kept virgin, mated once, or forced to cohabit with a male). We find no evidence that the economics of mating are determined by interactions between cytoplasmic genes expressed in females and nuclear genes expressed in males and, therefore, no support for a sexually antagonistic intergenomic arms race. The cost of mating to females was, however, shaped by an interaction between the cytoplasmic and nuclear genes expressed within females. Thus, cytonuclear interactions are embroiled in the economics of mating.
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| 7. |
- Dowling, Damian K., et al.
(author)
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Effects of cytoplasmic genes on sperm viability and sperm morphology in a seed beetle : Implications for sperm competition theory?
- 2007
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In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 20:1, s. 358-368
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Journal article (peer-reviewed)abstract
- Sperm competition theory predicts that sperm traits influencing male fertilizing ability will evolve adaptively. However, it has been suggested that some sperm traits may be at least partly encoded by mitochondrial genes. If true, this may constrain the adaptive evolution of such traits because mitochondrial DNA (mtDNA) is maternally inherited and there is thus no selection on mtDNA in males. Phenotypic variation in such traits may nevertheless be high because mutations in mtDNA that have deleterious effects on male traits, but neutral or beneficial effects in females, may be maintained by random processes or selection in females. We used backcrossing to create introgression lines of seed beetles (Callosobruchus maculatus), carrying orthogonal combinations of distinct lineages of cytoplasmic and nuclear genes, and then assayed sperm viability and sperm length in all lines. We found sizeable cytoplasmic effects on both sperm traits and our analyses also suggested that the cytoplasmic effects varied across nuclear genetic backgrounds. We discuss some potential implications of these findings for sperm competition theory.
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| 8. |
- Dowling, Damian K., et al.
(author)
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Evolutionary implications of non-neutral mitochondrial genetic variation
- 2008
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In: Trends in Ecology & Evolution. - : Cell Press. - 0169-5347 .- 1872-8383. ; 23:10, s. 546-554
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Research review (peer-reviewed)abstract
- Sequence variation in mitochondrial DNA (mtDNA) was traditionally considered to be selectively neutral. However, an accumulating body of evidence indicates that this assumption is invalid. Furthermore, recent advances indicate that mtDNA polymorphism can be maintained within populations via selection on the joint mitochondrial-nuclear genotype. Here, we review the latest findings that show mitochondrial and cytoplasmic genetic variation for life-history traits and fitness. We highlight the key importance of the mitochondrial-nuclear interaction as a unit of selection and discuss the consequences of mitochondrially encoded fitness effects on several key evolutionary processes. Our goal is to draw attention to the profound, yet neglected, influence of the mitochondrial genome on the fields of ecology and evolution.
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| 9. |
- Dowling, Damian k., et al.
(author)
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Intergenomic epistasis for fitness : Within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster
- 2007
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In: Genetics. - : Oxford University Press (OUP). - 0016-6731 .- 1943-2631. ; 175:1, s. 235-244
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Journal article (peer-reviewed)abstract
- The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.
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| 10. |
- Dowling, Damian K., et al.
(author)
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Red plumage and its association with reproductive success in red-capped robins
- 2006
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In: Annales Zoologici Fennici. - 0003-455X .- 1797-2450. ; 43:4, s. 311-321
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Journal article (peer-reviewed)abstract
- Red plumage is produced mainly by deposition of carotenoid'pigments into the feathers, and is assumed to be costly. Recent studies suggest red plumage may be a condition-dependent, sexually selected signal. To date, few studies have explored the relationship between carotenoid-based plumage colour and genetic (realised) reproductive success. This is despite the rarity of genetic monogamy among. avian mating systems. We studied. this-relationship. in the red-capped robin (Petroica goodenovii) across two breeding seasons, using spectrophotometric techniques, to score colour and molecular markers to assign paternity. Males with the highest. within-pair. reproductive success during the first season moulted into,the most colourful plumage at the conclusion of that season. We found;no such correlations, when using putative measures of reproductive success, underlining the importance of unambiguous paternity assignment. However, males that moulted into the most, colourful plumage did not go on to attain highest. reproductive success during-the, subsequent breeding season (while displaying this plumage). Instead, variation in male reproductive success was explained by male body condition and age. These results suggest that the information value of male-plumage colour is unpredictable.
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| 11. |
- Dowling, Damian K., et al.
(author)
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Temperature-specific outcomes of cytoplasmic-nuclear interactions on egg-to-adult development time in seed beetles
- 2007
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In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 61:1, s. 194-201
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Journal article (peer-reviewed)abstract
- The integration of the mitochondrial and nuclear genomes coordinates cellular energy production and is fundamental to life among eukaryotes. Therefore, there is potential for strong selection to shape the interactions between the two genomes. Several studies have now demonstrated that epistatic interactions between cytoplasmic and nuclear genes for fitness can occur both at a "within" and "across" population level. Genotype-by-environment interactions are common for traits that are encoded by nuclear genes, but the effects of environmental heterogeneity on traits that are partly encoded by cytoplasmic genes have received little attention despite the fact that there are reasons to believe that phenotypic effects of cytoplasmic genetic variation may often be environment specific. Consequently, the importance of environmental heterogeneity to the outcomes of cyto-nuclear fitness interactions and to the maintenance of mitochondrial polymorphism is unclear. Here, we assess the influence of temperature on cyto-nuclear effects on egg-to-adult development time in seed beetles (Callosobruchus maculatus). We employed an "across-population" design, sourcing beetles from five distinct populations and using backcrossing to create orthogonal combinations of distinct introgression lines, fixed for their cytoplasmic and nuclear lineages. We then assayed development times at two different temperatures and found sizeable cyto-nuclear effects in general, as well as temperature- and block-specific cyto-nuclear effects. These results demonstrate that environmental factors such as temperature do exert selection on cytoplasmic genes by favoring specific cyto-nuclear genetic combinations, and are consistent with the suggestion that complex genotype-by-environment interactions may promote the maintenance of polymorphism in mitochondrial genes.
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| 12. |
- Innocenti, Paolo, et al.
(author)
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Experimental Evidence Supports a Sex-Specific Selective Sieve in Mitochondrial Genome Evolution
- 2011
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In: Science. - : American Association for the Advancement of Science (AAAS). - 0036-8075 .- 1095-9203. ; 332:6031, s. 845-848
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Journal article (peer-reviewed)abstract
- Mitochondria are maternally transmitted; hence, their genome can only make a direct and adaptive response to selection through females, whereas males represent an evolutionary dead end. In theory, this creates a sex-specific selective sieve, enabling deleterious mutations to accumulate in mitochondrial genomes if they exert male-specific effects. We tested this hypothesis, expressing five mitochondrial variants alongside a standard nuclear genome in Drosophila melanogaster, and found striking sexual asymmetry in patterns of nuclear gene expression. Mitochondrial polymorphism had few effects on nuclear gene expression in females but major effects in males, modifying nearly 10% of transcripts. These were mostly male-biased in expression, with enrichment hotspots in the testes and accessory glands. Our results suggest an evolutionary mechanism that results in mitochondrial genomes harboring male-specific mutation loads.
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| 13. |
- Maklakov, Alexei A, et al.
(author)
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Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster
- 2006
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In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 60:10, s. 2081-2086
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Journal article (peer-reviewed)abstract
- It has been suggested that mitochondrial DNA (mtDNA) may play an important role in aging. Yet, few empirical studies have tested this hypothesis, partly because the degree of sequence polymorphism in mtDNA is assumed to be low. However, low sequence variation may not necessarily translate into low phenotypic variation. Here, we report an experiment that tests whether there is within-population variation in cytoplasmic genes for female longevity and senescence. To achieve this, we randomly selected 25 "mitochondrial founders" from a single, panmictic population of Drosophila melanogaster and used these founders to generate distinct "mt" lines in which we controlled for the nuclear background by successive backcrossing. Potential confounding effects of cytoplasmically transmitted bacteria were eliminated by tetracycline treatment. The mt lines were then assayed for differences in longevity, Gompertz intercept (frailty), and demographic rate of change in mortality with age (rate-of-senescence) in females. We found significant cytoplasmic effects on all three variables. This provides evidence that genetic variation in cytoplasmic genes, presumably mtDNA, contributes to variation in female mortality and aging.
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| 14. |
- Maklakov, Alexei A., et al.
(author)
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Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster
- 2006
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In: Evolution. - : The Society for the Study of Evolution. - 0014-3820 .- 1558-5646. ; 60:10, s. 2081-2086
-
Journal article (peer-reviewed)abstract
- It has been suggested that mitochondrial DNA (mtDNA) may play an important role in aging. Yet, few empirical studies have tested this hypothesis, partly because the degree of sequence polymorphism in mtDNA is assumed to be low. However, low sequence variation may not necessarily translate into low phenotypic variation. Here, we report an experiment that tests whether there is within-population variation in cytoplasmic genes for female longevity and senescence. To achieve this, we randomly selected 25 "mitochondrial founders" from a single, panmictic population of Drosophila melanogaster and used these founders to generate distinct "mt" lines in which we controlled for the nuclear background by successive backcrossing. Potential confounding effects of cytoplasmically transmitted bacteria were eliminated by tetracycline treatment. The mt lines were then assayed for differences in longevity, Gompertz intercept (frailty), and demographic rate of change in mortality with age (rate-of-senescence) in females. We found significant cytoplasmic effects on all three variables. This provides evidence that genetic variation in cytoplasmic genes, presumably mtDNA, contributes to variation in female mortality and aging.
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| 15. |
- Rogell, Björn, et al.
(author)
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Controlling for body size leads to inferential biases in the biological sciences
- 2020
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In: Evolution Letters. - : Oxford University Press (OUP). - 2056-3744. ; 4:1, s. 73-82
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Journal article (peer-reviewed)abstract
- Many traits correlate with body size. Studies that seek to uncover the ecological factors that drive evolutionary responses in traits typically examine these responses relative to associated changes in body size using multiple regression analysis. However, it is not well appreciated that in the presence of strongly correlated variables, the partial (i.e., relative) regression coefficients often change sign compared to the original coefficients. Such sign reversals are difficult to interpret in a biologically meaningful way, and could lead to erroneous evolutionary inferences if the true mechanism underlying the sign reversal differed from the proposed mechanism. Here, we use simulations to demonstrate that sign reversal occurs over a wide range of parameter values common in the biological sciences. Further, as a case-in-point, we review the literature on brain size evolution; a field that explores how ecological traits relate to the evolution of relative brain size (brain size relative to body size). We find that most studies show sign reversals and thus that the inferences of many studies in this field may be inconclusive. Finally, we propose some approaches to mitigating this issue.
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