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1.
  • Bolund, Elisabeth, et al. (author)
  • Reduced costs of reproduction in females mediate a shift from a male-biased to a female-biased lifespan in humans
  • 2016
  • In: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 6
  • Journal article (peer-reviewed)abstract
    • The causes underlying sex differences in lifespan are strongly debated. While females commonly outlive males in humans, this is generally less pronounced in societies before the demographic transition to low mortality and fertility rates. Life-history theory suggests that reduced reproduction should benefit female lifespan when females pay higher costs of reproduction than males. Using unique longitudinal demographic records on 140,600 reproducing individuals from the Utah Population Database, we demonstrate a shift from male-biased to female-biased adult lifespans in individuals born before versus during the demographic transition. Only women paid a cost of reproduction in terms of shortened post-reproductive lifespan at high parities. Therefore, as fertility decreased over time, female lifespan increased, while male lifespan remained largely stable, supporting the theory that differential costs of reproduction in the two sexes result in the shifting patterns of sex differences in lifespan across human populations. Further, our results have important implications for demographic forecasts in human populations and advance our understanding of lifespan evolution.
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2.
  • Alavioon, Ghazal, 1986-, et al. (author)
  • Within-ejaculate selection for sperm longevity reduces male reproductive ageing
  • Other publication (other academic/artistic)abstract
    • Males produce numerous sperm in the single ejaculate that greatly outnumber their potential egg targets. Recent studies found that phenotypic variation among sperm in the single ejaculate of a male reflects the phenotype and the genotype of the resulting offspring. Specifically, within-ejaculate sperm selection (WESS) for sperm longevity increased the performance of the resulting offspring in several key life-history traits in early-life. Because increased early-life reproductive performance often correlates with rapid ageing, it is possible that WESS increases early-life fitness at the cost of accelerated senescence. Alternatively, WESS can improve offspring quality throughout the life cycle, including reduced age-specific deterioration. We found that WESS for sperm longevity reduced age-specific deterioration of male fertility and embryo survival, while there is no effect on fertilization success. Remarkably, we found opposing effect of WESS on female fecundity, where selection for sperm longevity resulted in increased early-life performance followed by a slow decline, while unselected controls started low but increased their fecundity with age. Intriguingly, WESS also reduced the age-specific decline in fertilization success in females, suggesting that selection for sperm longevity improves at least some aspects of female reproductive ageing. These results demonstrate that within-ejaculate variation in sperm phenotype contributes to individual variation in animal life histories in the two sexes and have important implications for assisted fertilization programs in livestock and humans. 
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3.
  • Berg, Elena C., et al. (author)
  • Kin but less than kind : within-group male relatedness does not increase female fitness in seed beetles
  • 2019
  • In: Proceedings of the Royal Society of London. Biological Sciences. - : ROYAL SOC. - 0962-8452 .- 1471-2954. ; 286:1910, s. 1471-2954
  • Journal article (peer-reviewed)abstract
    • Theory maintains within-group male relatedness can mediate sexual conflict by reducing male-male. competition and collateral harm to females. We tested whether male relatedness can lessen female harm in the seed beetle Callosobruchus maculatus. Male relatedness did not influence female lifetime reproductive success or individual fitness across two different ecologically relevant scenarios of mating competition. However, male relatedness marginally improved female survival. Because male relatedness improved female-survival in late life when C. maculatus females are no longer producing offspring, our results do not provide support for the role of within-group male relatedness in mediating sexual conflict. The fact that male relatedness improves the post-reproductive part of the female life cycle strongly suggests that the effect is non-adaptive. We discuss adaptive and non-adaptive mechanisms that could result in reduced female harm in this and previous studies, and suggest that cognitive error is a likely explanation.
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4.
  • Berg, Elena C., et al. (author)
  • Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle
  • 2012
  • In: Proceedings of the Royal Society of London. Biological Sciences. - : The Royal Society. - 0962-8452 .- 1471-2954. ; 279:1745, s. 4296-4302
  • Journal article (peer-reviewed)abstract
    • Males and females have different routes to successful reproduction, resulting in sex differences in lifespan and age-specific allocation of reproductive effort. The trade-off between current and future reproduction is often resolved differently by males and females, and both sexes can be constrained in their ability to reach their sex-specific optima owing to intralocus sexual conflict. Such genetic antagonism may have profound implications for evolution, but its role in ageing and lifespan remains unresolved. We provide direct experimental evidence that males live longer and females live shorter than necessary to maximize their relative fitness in Callosobruchus maculatus seed beetles. Using artificial selection in a genetically heterogeneous population, we created replicate long-life lines where males lived on average 27 per cent longer than in short-life lines. As predicted by theory, subsequent assays revealed that upward selection on male lifespan decreased relative male fitness but increased relative female fitness compared with downward selection. Thus, we demonstrate that lifespan-extending genes can help one sex while harming the other. Our results show that sexual antagonism constrains adaptive life-history evolution, support a novel way of maintaining genetic variation for lifespan and argue for better integration of sex effects into applied research programmes aimed at lifespan extension.
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5.
  • Berger, David, et al. (author)
  • Intralocus Sexual Conflict and Environmental Stress
  • 2014
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 68:8, s. 2184-2196
  • Journal article (peer-reviewed)abstract
    • Intralocus sexual conflict (IaSC) occurs when selection at a given locus favors different alleles in males and females, placing a fundamental constraint on adaptation. However, the relative impact of IaSC on adaptation may become reduced in stressful environments that expose conditionally deleterious mutations to selection. The genetic correlation for fitness between males and females (r(MF)) provides a quantification of IaSC across the genome. We compared IaSC at a benign (29 degrees C) and a stressful (36 degrees C) temperature by estimating r(MF)s in two natural populations of the seed beetle Callosobruchus maculatus using isofemale lines. In one population, we found substantial IaSC under benign conditions signified by a negative r(MF) (-0.51) and, as predicted, a significant reduction of IaSC under stress signified by a reversed and positive r(MF) (0.21). The other population displayed low IaSC at both temperatures (r(MF): 0.38; 0.40). In both populations, isofemale lines harboring alleles beneficial to males but detrimental to females at benign conditions tended to show overall low fitness under stress. These results offer support for low IaSC under stress and suggest that environmentally sensitive and conditionally deleterious alleles that are sexually selected in males mediate changes in IaSC. We discuss implications for adaptive evolution in sexually reproducing populations.
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6.
  • Berger, David, et al. (author)
  • Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles
  • 2016
  • In: American Naturalist. - : University of Chicago Press. - 0003-0147 .- 1537-5323. ; 188:4, s. E98-E112
  • Journal article (peer-reviewed)abstract
    • The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history andmorphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individuallevel sex-specific selection and population demography and places lifehistory traits at the epicenter of these dynamics.
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7.
  • Berger, David, et al. (author)
  • Multivariate intralocus sexual conflict in seed beetles
  • 2014
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 68:12, s. 3457-69
  • Journal article (peer-reviewed)abstract
    • Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex-specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life-history syndrome in many species. Male-limited selection for short life span led to correlated evolution in females toward a more male-like multivariate phenotype. Conversely, males selected for long life span became more female-like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short-life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex-specific genetic architecture.
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8.
  • Berger, David, et al. (author)
  • Sexually antagonistic selection on genetic variation underlying both male and female same-sex sexual behavior
  • 2016
  • In: BMC Evolutionary Biology. - : Springer Science and Business Media LLC. - 1471-2148. ; 16
  • Journal article (peer-reviewed)abstract
    • Intralocus sexual conflict, arising from selection for different alleles at the same locus in males and females, imposes a constraint on sex-specific adaptation. Intralocus sexual conflict can be alleviated by the evolution of sex-limited genetic architectures and phenotypic expression, but pleiotropic constraints may hinder this process. Here, we explored putative intralocus sexual conflict and genetic (co)variance in a poorly understood behavior with near male-limited expression. Same-sex sexual behaviors (SSBs) generally do not conform to classic evolutionary models of adaptation but are common in male animals and have been hypothesized to result from perception errors and selection for high male mating rates. However, perspectives incorporating sex-specific selection on genes shared by males and females to explain the expression and evolution of SSBs have largely been neglected.
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9.
  • Bilde, Trine, et al. (author)
  • Sex differences in the genetic architecture of lifespan in a seed beetle : extreme inbreeding extends male lifespan
  • 2009
  • In: BMC Evolutionary Biology. - : Springer Science and Business Media LLC. - 1471-2148. ; 9, s. 33-
  • Journal article (peer-reviewed)abstract
    • Background: Sex differences in lifespan are ubiquitous throughout the animal kingdom but the causes underlying this phenomenon remain poorly understood. Several explanations based on asymmetrical inheritance patterns (sex chromosomes or mitochondrial DNA) have been proposed, but these ideas have rarely been tested experimentally. Alternatively, sexual dimorphism in lifespan could result from sex-specific selection, caused by fundamental differences in how males and females optimize their fitness by allocating resources into current and future reproduction. Results: Here we used sex-specific responses to inbreeding to study the genetic architecture of lifespan and mortality rates in Callosobruchus maculatus, a seed beetle that shows sexual dimorphism in lifespan. Two independent assays revealed opposing sex-specific responses to inbreeding. The combined data set showed that inbred males live longer than outbred males, while females show the opposite pattern. Both sexes suffered reduced fitness measured as lifetime reproductive success as a result of inbreeding. Conclusion: No model based on asymmetrical inheritance can explain increased male lifespan in response to inbreeding. Our results are however compatible with models based on sex-specific selection on reproductive strategies. We therefore suggest that sex-specific differences in lifespan in this species primarily result from sexually divergent selection.
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10.
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11.
  • Burgevin, Lorraine, et al. (author)
  • Intersexual correlation for same-sex sexual behaviour in an insect
  • 2013
  • In: Animal Behaviour. - : Elsevier BV. - 0003-3472 .- 1095-8282. ; 85:4, s. 759-762
  • Journal article (peer-reviewed)abstract
    • Same-sex sexual behaviour is widespread across taxa and is particularly common in insects, in which up to 50% of copulation attempts by males are directed towards other males in some species. Research effort has focused on male-male same-sex behaviour and the prevailing theory is that benefits of high mating rate combined with poor sex discrimination explain the high incidence of male-male mounting. However, the evolution of female-female mounting is more enigmatic, since females typically do not mount males in order to mate. Using a full-sib design, we found an intersexual correlation for same-sex mounting in the beetle Callosobruchus maculatus. Variation in male-male mounting across families explained over 20% of variation in female-female mounting. Moreover, we found no evidence that same-sex behaviour was related to general activity level in either sex or carried a fitness cost to females. Taken together, our results suggest that female-female mounting is a relatively low-cost behaviour that may be maintained in the population via selection on males.
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12.
  • Cayetano, Luis, et al. (author)
  • Evolution of male and female genitalia following release from sexual selection
  • 2011
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 65:8, s. 2171-2183
  • Journal article (peer-reviewed)abstract
    • Despite the key functions of the genitalia in sexual interactions and fertilization, the role of sexual selection and conflict in shaping genital traits remains poorly understood. Seed beetle (Callosobruchus maculatus) males possess spines on the intromittent organ, and females possess a thickened reproductive tract wall that also bears spines. We investigated the role of sexual selection and conflict by imposing monogamous mating on eight replicate populations of this naturally polygamous insect, while maintaining eight other populations under polygamy. To establish whether responses to mating system manipulation were robust to ecological context, we simultaneously manipulated life-history selection (early/late reproduction). Over 18-21 generations, male genital spines evolved relatively reduced length in large males (i.e., shallower static allometry) in monogamous populations. Two nonintromittent male genital appendages also evolved in response to the interaction of mating system and ecology. In contrast, no detectable evolution occurred in female genitalia, consistent with the expectation of a delayed response in defensive traits. Our results support a sexually antagonistic role for the male genital spines, and demonstrate the evolution of static allometry in response to variation in sexual selection opportunity. We argue that further advances in the study of genital coevolution will require a much more detailed understanding of the functions of male and female genital traits.
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13.
  • Chen, Hwei-yen, 1983-, et al. (author)
  • Condition dependence of male mortality drives the evolution of sex differences in longevity
  • 2014
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 24:20, s. 2423-2427
  • Journal article (peer-reviewed)abstract
    • Males and females age at different rates and have different life expectancies across the animal kingdom, but what causes the longevity "gender gaps" remains one of the most fiercely debated puzzles among biologists and demographers [1-7]. Classic theory predicts that the sex experiencing higher rate of extrinsic mortality evolves faster aging and reduced longevity [1]. However, condition dependence of mortality [8, 9] can counter this effect by selecting against senescence in whole-organism performance [5, 10]. Contrary to the prevailing view but in line with an emerging new theory [7-9, 11], we show that the evolution of sex difference in longevity depends on the factors that cause sex-specific mortality and cannot be predicted from the mortality rate alone. Experimental evolution in an obligately sexual roundworm, Caenorhabditis remanei, in which males live longer than females, reveals that sexual dimorphism in longevity erodes rapidly when the extrinsic mortality in males is increased at random. We thus experimentally demonstrate evolution of the sexual monomorphism in longevity in a sexually dimorphic organism. Strikingly, when extrinsic mortalityis increased in a way that favors survival of fast-moving individuals, males evolve increased longevities, thereby widening the gender gap. Thus,sex-specific selection on whole-organism performance in males renders them less prone to the ravages of old age than females, despite higher rates of extrinsic mortality. Our results reconcile previous research with recent theoretical breakthroughs [8, 9] by showing that sexual dimorphism inlongevity evolves rapidly and predictably as a result of the sex-specific interactions between environmental hazard and organism's condition.
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14.
  • Chen, Hwei -Yen, et al. (author)
  • Evolution of male age-specific reproduction under differential risks and causes of death : males pay the cost of high female fitness
  • 2016
  • In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 29:4, s. 848-856
  • Journal article (peer-reviewed)abstract
    • Classic theories of ageing evolution predict that increased extrinsic mortality due to an environmental hazard selects for increased early reproduction, rapid ageing and short intrinsic lifespan. Conversely, emerging theory maintains that when ageing increases susceptibility to an environmental hazard, increased mortality due to this hazard can select against ageing in physiological condition and prolong intrinsic lifespan. However, evolution of slow ageing under high-condition-dependent mortality is expected to result from reallocation of resources to different traits and such reallocation may be hampered by sex-specific trade-offs. Because same life-history trait values often have different fitness consequences in males and females, sexually antagonistic selection can preserve genetic variance for lifespan and ageing. We previously showed that increased condition-dependent mortality caused by heat shock leads to evolution of long-life, decelerated late-life mortality in both sexes and increased female fecundity in the nematode, Caenorhabditis remanei. Here, we used these cryopreserved lines to show that males evolving under heat shock suffered from reduced early-life and net reproduction, while mortality rate had no effect. Our results suggest that heat-shock resistance and associated long-life trade-off with male, but not female, reproduction and therefore sexually antagonistic selection contributes to maintenance of genetic variation for lifespan and fitness in this population.
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15.
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16.
  • Chen, Hwei-yen, 1983-, et al. (author)
  • Germline mutation rate is elevated in young and old parents in Caenorhabditis remanei
  • 2023
  • In: Evolution Letters. - : Oxford University Press. - 2056-3744. ; 7:6, s. 478-489
  • Journal article (peer-reviewed)abstract
    • The effect of parental age on germline mutation rate across generations is not fully understood. While some studies report a positive linear relationship of mutation rate with increasing age, others suggest that mutation rate varies with age but not in a linear fashion. We investigated the effect of parental age on germline mutations by generating replicated mutation accumulation lines in Caenorhabditis remanei at three parental ages ("Young T1" [Day 1], "Peak T2" [Day 2], and "Old T5" [Day 5] parents). We conducted whole-genome resequencing and variant calling to compare differences in mutation rates after three generations of mutation accumulation. We found that Peak T2 lines had an overall reduced mutation rate compared to Young T1 and Old T5 lines, but this pattern of the effect varied depending on the variant impact. Specifically, we found no high-impact variants in Peak T2 lines, and modifiers and up- and downstream gene variants were less frequent in these lines. These results suggest that animals at the peak of reproduction have better DNA maintenance and repair compared to young and old animals. We propose that C. remanei start to reproduce before they optimize their DNA maintenance and repair, trading the benefits of earlier onset of reproduction against offspring mutation load. The increase in offspring mutation load with age likely represents germline senescence. Germline mutations play a key role in evolution through the generation of novel genotypes. Estimating the mutation rate in species, populations, and individuals is one way to understand the relative timeframe of evolutionary processes, for the timing of historical events and for estimating heritability of traits and diseases. Individual age at reproduction is known to affect the number of mutations being transferred into the next generation and generally mutation rate is thought to increase with increasing parental age. However, preventing mutations in germ cells is potentially costly and it may pay off to optimize germline genome repair and maintenance during peak reproductive periods, and relax it during nonpeak periods. This idea has been put forward to explain for example the reduction of gonad size in seasonally reproducing animals during nonreproductive periods and supported by the finding that the mutation rate seems to be higher in teenage men compared to men during their peak reproductive ages. We further tested this idea of a nonlinear relationship between age and mutation rate by performing a mutation accumulation experiment in a short-lived nematode. We kept experimental lines and allowed adults to reproduce at different ages in different lines, with some lines reproducing before, some during, and some after their reproductive peak. We found that mutation rates are higher in nematode lines reproducing before or after the reproductive peak compared to those reproducing during the peak. Our results therefore support the idea that germline genome maintenance and repair is potentially costly and that the mutation rate does not just increase with age but is optimized during the peak reproductive age of an organism.
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17.
  • Chen, Hwei-yen, et al. (author)
  • The worm that lived : evolution of rapid aging under high extrinsic mortality revisited
  • 2013
  • In: Worm. - : Informa UK Limited. - 2162-4054. ; 2:3
  • Journal article (peer-reviewed)abstract
    • Organisms age because of the “selection shadow”—the decline of the force of natural selection with age. Seemingly straightforward corollary of this theory is the Medawar-Williams prediction, which maintains that increased extrinsic (non-aging) mortality will result in the evolution of accelerated aging and decreased longevity. Despite its centrality to modern thinking about the ultimate causes of aging, this prediction ignores the fact that mortality is often a non-random process depending on individual condition. Increased condition-dependent mortality inescapably results in increased selection for resistance against the agent of mortality. Provided that resistance to various stressors is commonly associated with increased longevity, the evolutionary outcome is no longer certain. We recently documented this experimentally by showing that populations of Caenorhabditis remanei evolved to live shorter under high extrinsic mortality, but only when mortality was applied haphazardly. On the contrary, when extrinsic mortality was caused by heat-shock, populations experiencing the same rate of increased mortality evolved greater longevities, notwithstanding increased “selection shadow.” Intriguingly, stress-resistant and long-lived worms were also more fecund. We discuss these results in the light of recent theoretical developments, such as condition-environment interactions and hyperfunction theory of aging.
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18.
  • Chen, Hwei-yen, et al. (author)
  • Why ageing stops : heterogeneity explains late-life mortality deceleration in nematodes
  • 2013
  • In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 9:5, s. 20130217-
  • Journal article (peer-reviewed)abstract
    • While ageing is commonly associated with exponential increase in mortality with age, mortality rates paradoxically decelerate late in life resulting in distinct mortality plateaus. Late-life mortality plateaus have been discovered in a broad variety of taxa, including humans, but their origin is hotly debated. One hypothesis argues that deceleration occurs because the individual probability of death stops increasing at very old ages, predicting the evolution of earlier onset of mortality plateaus under increased rate of extrinsic mortality. By contrast, heterogeneity theory suggests that mortality deceleration arises from individual differences in intrinsic lifelong robustness and predicts that variation in robustness between populations will result in differences in mortality deceleration. We used experimental evolution to directly test these predictions by independently manipulating extrinsic mortality rate (high or low) and mortality source (random death or condition-dependent) to create replicate populations of nematodes, Caenorhabditis remanei that differ in the strength of selection in late-life and in the level of lifelong robustness. Late-life mortality deceleration evolved in response to differences in mortality source when mortality rate was held constant, while there was no consistent response to differences in mortality rate. These results provide direct experimental support for the heterogeneity theory of late-life mortality deceleration.
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19.
  • Fricke, Claudia, et al. (author)
  • Male age does not affect female fitness in a polyandrous beetle, Callosobruchus maculatus
  • 2007
  • In: Animal Behaviour. - : Elsevier BV. - 0003-3472 .- 1095-8282. ; 74:3, s. 541-548
  • Journal article (peer-reviewed)abstract
    • Males in different taxa are likely to suffer from a reduction in the quantity and/or quality of their sperm with age. This predicts age-related direct and indirect effects on female fitness. Hence, females may be selected to avoid matings with old males, or to employ alternative mating tactics, such as polyandry, to avoid fertilization by sperm of older males. In contrast, ‘viability indicator’ models of mate choice predict female preference for old males that have proven their survival ability and signal more reliably. We used a polygamous seed beetle, Callosobruchus maculatus, to test for the effects of male age on male mating success and examine the relationship between male age and female fitness, measured as female life span, lifetime fecundity, hatching success of eggs, larval development rate and egg-to-adult survival of offspring. Furthermore, we tested the hypothesis that polyandry may protect females against low numbers of functional sperm produced by old males. We report, contrary to previous findings, that male mating success indeed decreases with male age in this species. However, mating with older males did not in any way compromise female fitness and, consequently, we found no support for the idea that polyandry helps females reduce any costs of mating with older males.
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20.
  • Hooper, Amy K., et al. (author)
  • Ontogenetic timing as a condition-dependent life history trait : High-condition males develop quickly, peak early, and age fast
  • 2017
  • In: Evolution. - : WILEY. - 0014-3820 .- 1558-5646. ; 71:3, s. 671-685
  • Journal article (peer-reviewed)abstract
    • Within-population variation in ageing remains poorly understood. In males, condition-dependent investment in secondary sexual traits may incur costs that limit ability to invest in somatic maintenance. Moreover, males often express morphological and behavioral secondary sexual traits simultaneously, but the relative effects on ageing of investment in these traits remain unclear. We investigated the condition dependence of male life history in the neriid fly Telostylinus angusticollis. Using a fully factorial design, we manipulated male early-life condition by varying nutrient content of the larval diet and, subsequently, manipulated opportunity for adult males to interact with rival males. We found that high-condition males developed more quickly and reached their reproductive peak earlier in life, but also experienced faster reproductive ageing and died sooner than low-condition males. By contrast, interactions with rival males reduced male lifespan but did not affect male reproductive ageing. High-condition in early life is therefore associated with rapid ageing in T. angusticollis males, even in the absence of damaging male-male interactions. Our results show that abundant resources during the juvenile phase are used to expedite growth and development and enhance early-life reproductive performance at the expense of late-life performance and survival, demonstrating a clear link between male condition and ageing.
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21.
  • Jiménez-Ortega, Dante, et al. (author)
  • Long life evolves in large-brained bird lineages
  • 2020
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 74:12, s. 2617-2628
  • Journal article (peer-reviewed)abstract
    • The brain is an energetically costly organ that consumes a disproportionate amount of resources. Species with larger brains relative to their body size have slower life histories, with reduced output per reproductive event and delayed development times that can be offset by increasing behavioral flexibility. The cognitive buffer hypothesis maintains that large brain size decreases extrinsic mortality due to greater behavioral flexibility, leading to a longer lifespan. Alternatively, slow life histories, and long lifespan can be a pre-adaptation for the evolution of larger brains. Here, we use phylogenetic path analysis to contrast different evolutionary scenarios and disentangle direct and indirect relationships between brain size, body size, life history, and longevity across 339 altricial and precocial bird species. Our results support both a direct causal link between brain size and lifespan, and an indirect effect via other life history traits. These results indicate that large brain size engenders longer life, as proposed by the cognitive buffer hypothesis.
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22.
  • Kotrschal, Alexander, et al. (author)
  • Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain
  • 2013
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 23:2, s. 168-171
  • Journal article (peer-reviewed)abstract
    • The large variation in brain size that exists in the animal kingdom has been suggested to have evolved through the balance between selective advantages of greater cognitive ability and the prohibitively high energy demands of a larger brain (the "expensive-tissue hypothesis" [1]). Despite over a century of research on the evolution of brain size, empirical support for the trade-off between cognitive ability and energetic costs is based exclusively on correlative evidence [2], and the theory remains controversial [3, 4]. Here we provide experimental evidence for costs and benefits of increased brain size. We used artificial selection for large and small brain size relative to body size in a live-bearing fish, the guppy (Poecilia reticulata), and found that relative brain size evolved rapidly in response to divergent selection in both sexes. Large-brained females outperformed small-brained females in a numerical learning assay designed to test cognitive ability. Moreover, large-brained lines, especially males, developed smaller guts, as predicted by the expensive-tissue hypothesis [1], and produced fewer offspring. We propose that the evolution of brain size is mediated by a functional trade-off between increased cognitive ability and reproductive performance and discuss the implications of these findings for vertebrate brain evolution.
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23.
  • Kotrschal, Alexander, et al. (author)
  • Artificial Selection on Relative Brain Size Reveals a Positive Genetic Correlation Between Brain Size and Proactive Personality in the Guppy
  • 2014
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 68:4, s. 1139-1149
  • Journal article (peer-reviewed)abstract
    • Animal personalities range from individuals that are shy, cautious, and easily stressed (a "reactive" personality type) to individuals that are bold, innovative, and quick to learn novel tasks, but also prone to routine formation (a "proactive" personality type). Although personality differences should have important consequences for fitness, their underlying mechanisms remain poorly understood. Here, we investigated how genetic variation in brain size affects personality. We put selection lines of large- and small-brained guppies (Poecilia reticulata), with known differences in cognitive ability, through three standard personality assays. First, we found that large-brained animals were faster to habituate to, and more exploratory in, open field tests. Large-brained females were also bolder. Second, large-brained animals excreted less cortisol in a stressful situation (confinement). Third, large-brained animals were slower to feed from a novel food source, which we interpret as being caused by reduced behavioral flexibility rather than lack of innovation in the large-brained lines. Overall, the results point toward a more proactive personality type in large-brained animals. Thus, this study provides the first experimental evidence linking brain size and personality, an interaction that may affect important fitness-related aspects of ecology such as dispersal and niche exploration.
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24.
  • Kotrschal, Alexander, et al. (author)
  • Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size
  • 2015
  • In: Journal of Evolutionary Biology. - : Wiley. - 1010-061X .- 1420-9101. ; 28:4, s. 841-850
  • Journal article (peer-reviewed)abstract
    • Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade-offs between brain size and sexual traits. Instead, larger-brained males had higher expression of several primary and precopulatory sexual traits - they had longer genitalia, were more colourful and developed longer tails than smaller-brained males. Larger-brained males were also in better body condition when housed in single-sex groups. There was no difference in post-copulatory sexual traits between males from the large- and small-brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.
  •  
25.
  • Kotrschal, Alexander, et al. (author)
  • Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata
  • 2012
  • In: Behavioral Ecology and Sociobiology. - : Springer Science and Business Media LLC. - 0340-5443 .- 1432-0762. ; 66:11, s. 1485-1492
  • Journal article (peer-reviewed)abstract
    • The vertebrate brain is a remarkably plastic organ, which responds quickly to environmental changes. However, to date, studies investigating plasticity in brain morphology have focused mostly on the physical properties of the surrounding environment, and little is known about brain plasticity in response to the social environment. Moreover, sex differences in brain plasticity remain virtually unexplored. Here, we tested how the social environment influenced brain morphology in adult males and females using experimental manipulation of the sex composition of social pairs (same sex vs. mixed sex) in the guppy (Poecilia reticulata). We detected substantial sex-specific plasticity in both the overall brain size (controlling for body size) and separate brain structures. The brain size was larger in males that interacted with females, and female optic tectum was larger in female-only groups. Overall, females had larger olfactory bulbs and cerebellum in comparison to males. While net sexual dimorphism in the brain structure can be explained in light of the known differences in boldness and foraging behaviour between the sexes, our results also support that cognitive demands associated with courtship behaviour can lead to plastic changes in the brain size. Our findings demonstrate that not only social environment can generate rapid, plastic responses in the vertebrate brain but also that such responses can depend strongly on sex.
  •  
26.
  •  
27.
  • Lind, Martin I., Dr, et al. (author)
  • Cost-free lifespan extension via optimization of gene expression in adulthood aligns with the developmental theory of ageing
  • 2021
  • In: Proceedings of the Royal Society of London. Biological Sciences. - : Royal Society. - 0962-8452 .- 1471-2954. ; 288:1944
  • Journal article (peer-reviewed)abstract
    • Ageing evolves because the force of selection on traits declines with age but the proximate causes of ageing are incompletely understood. The 'disposable soma' theory of ageing (DST) upholds that competitive resource allocation between reproduction and somatic maintenance underpins the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood. While the DST predicts the trade-off between reproduction and lifespan, the DTA predicts that age-specific optimization of gene expression can increase lifespan without reproduction costs. Here we investigated the consequences for lifespan, reproduction, egg size and individual fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five 'longevity' genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period increases lifespan, while we found limited evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression in adulthood often contributes to reduced lifespan directly rather than through competitive resource allocation between reproduction and somatic maintenance. Therefore, age-specific optimization of gene expression in evolutionarily conserved signalling pathways that regulate organismal life histories can increase lifespan without fitness costs.
  •  
28.
  • Lind, Martin I., Dr, 1980-, et al. (author)
  • Environmental variation mediates the evolution of anticipatory parental effects
  • 2020
  • In: Evolution Letters. - Oxford : John Wiley & Sons. - 2056-3744. ; 4:4, s. 371-381
  • Journal article (peer-reviewed)abstract
    • Theory maintains that when future environment is predictable, parents should adjust the phenotype of their offspring to match the anticipated environment. The plausibility of positive anticipatory parental effects is hotly debated and the experimental evidence for the evolution of such effects is currently lacking. We experimentally investigated the evolution of anticipatory maternal effects in a range of environments that differ drastically in how predictable they are. Populations of the nematode Caenorhabditis remanei, adapted to 20°C, were exposed to a novel temperature (25°C) for 30 generations with either positive or zero correlation between parent and offspring environment. We found that populations evolving in novel environments that were predictable across generations evolved a positive anticipatory maternal effect, because they required maternal exposure to 25°C to achieve maximum reproduction in that temperature. In contrast, populations evolving under zero environmental correlation had lost this anticipatory maternal effect. Similar but weaker patterns were found if instead rate-sensitive population growth was used as a fitness measure. These findings demonstrate that anticipatory parental effects evolve in response to environmental change so that ill-fitting parental effects can be rapidly lost. Evolution of positive anticipatory parental effects can aid population viability in rapidly changing but predictable environments. © 2020 The Authors. Evolution Letters published by Wiley Periodicals LLC on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB).
  •  
29.
  • Lind, Martin I., et al. (author)
  • Evolution of differential maternal age effects on male and female offspring development and longevity
  • 2015
  • In: Functional Ecology. - : Wiley. - 0269-8463 .- 1365-2435. ; 29:1, s. 104-110
  • Journal article (peer-reviewed)abstract
    • Maternal age effects on life-history traits, including longevity, are widespread and can be seen as a manifestation of ageing. However, little is known about how maternal life span may influence the maternal age effect. At a given chronological age, a long-lived parent may be at a younger biological age than a short-lived parent and thus has a less severe parental age effect. However, earlier work using experimentally evolved short- and long-lived lines did not support this hypothesis. We scored developmental time and longevity of 14995 individual seed beetles, Callosobruchus maculatus derived from replicate short-lived and long-lived lines created via artificial selection on male life span. Offspring from older mothers had shorter life span, which is consistent with most of the literature. We found support for the hypothesis that detrimental maternal age effects evolve to be weaker under selection for long life span. However, this finding was only apparent in males, suggesting that maternal age affects male and female offspring differently. These results suggest that sex-dependent parental age effects should be incorporated in the studies of longevity and ageing evolution and that selection on one sex can cause evolution of parental age effects in the other sex.
  •  
30.
  • Lind, Martin I., et al. (author)
  • Rapamycin additively extends lifespan in short- and long-lived lines of the nematode Caenorhabditis remanei
  • 2017
  • In: Experimental Gerontology. - : Elsevier BV. - 0531-5565 .- 1873-6815. ; 90, s. 79-82
  • Journal article (peer-reviewed)abstract
    • Despite tremendous progress in finding genes that, when manipulated, affects lifespan, little is known about the genetics underlying natural variation in lifespan. While segregating genetic variants for lifespan has been notoriously difficult to find in genome-wide association studies (GWAS), a complementary approach is to manipulate key genetic pathways in lines that differ in lifespan. If these candidate pathways are down regulated in long-lived lines, these lines can be predicted to respond less to pharmaceutical down-regulation of these pathways than short-lived lines. Experimental studies have identified the nutrient-sensing pathway TOR as a key regulator of lifespan in model organisms, and this pathway can effectively be down regulated using the drug rapamycin, which extends lifespan in all tested species. We expose short-and long-lived lines of the nematode Caenorhabditis remanei to rapamycin, and investigate if long-lived lines, which are hypothesized to already have down-regulated TOR signaling, respond less to rapamycin. We found no interaction between line and rapamycin treatment, since rapamycin extended lifespan independent of the intrinsic lifespan of the lines. This shows that rapamycin is equally effective on long and short-lived lines, and suggests that the evolution of long life may involve more factors that down-regulation of TOR.
  •  
31.
  • Lind, Martin I., 1980-, et al. (author)
  • Sex-specific growth and lifespan effects of germline removal in the dioecious nematode Caenorhabditis remanei
  • 2023
  • Other publication (other academic/artistic)abstract
    • Germline regulates the expression of life-history traits and mediates the trade-off between reproduction and somatic maintenance. However, germline maintenance in itself can be costly, and the costs can vary between the sexes depending on the number of gametes produced across the lifetime. We tested this directly by germline ablation using glp-1 RNAi in a dioecious nematode Caenorhabditis remanei. Germline removal strongly increased heat-shock resistance in both sexes, thus confirming the role of the germline in regulating somatic maintenance. However, germline removal resulted in increased lifespan only in males. High costs of mating strongly reduced lifespan in both sexes and obliterated the survival benefit of germline-less males even though neither sex produced any offspring. Furthermore, germline removal reduced male growth before maturation but not in adulthood, while female growth rate was reduced both before and especially after maturation. Thus, germline removal improves male lifespan without major growth costs, while germline-less females grow slower and do not live longer than reproductively functional counterparts in the absence of environmental stress. Overall, these results suggest that germline maintenance is costlier for males than for females.
  •  
32.
  • Lind, Martin I., et al. (author)
  • Sex-specific Tradeoffs With Growth and Fitness Following Life-span Extension by Rapamycin in an Outcrossing Nematode, Caenorhabditis remanei
  • 2016
  • In: The journals of gerontology. Series A, Biological sciences and medical sciences. - : Oxford University Press (OUP). - 1079-5006 .- 1758-535X. ; 71:7, s. 882-890
  • Journal article (peer-reviewed)abstract
    • Rapamycin inhibits the nutrient-sensing TOR pathway and extends life span in a wide range of organisms. Although life-span extension usually differs between the sexes, the reason for this is poorly understood. Because TOR influences growth, rapamycin likely affects life-history traits such as growth and reproduction. Sexes have different life-history strategies, and theory predicts that they will resolve the tradeoffs between growth, reproduction, and life span differently. Specifically, in taxa with female-biased sexual size dimorphism, reduced growth may have smaller effects on male fitness. We investigated the effects of juvenile, adult, or life-long rapamycin treatment on growth, reproduction, life span, and individual fitness in the outcrossing nematode Caenorhabditis remanei. Life-long exposure to rapamycin always resulted in the strongest response, whereas postreproductive exposure did not affect life span. Although rapamycin resulted in longer life span and smaller size in males, male individual fitness was not affected. In contrast, size and fitness were negatively affected in females, whereas life span was only extended under high rapamycin concentrations. Our results support the hypothesis that rapamycin affects key life-history traits in a sex-specific manner. We argue that the fitness cost of life-span extension will be sex specific and propose that the smaller sex generally pay less while enjoying stronger life-span increase.
  •  
33.
  • Lind, Martin I., et al. (author)
  • Slow development as an evolutionary cost of long life
  • 2017
  • In: Functional Ecology. - : Wiley. - 0269-8463 .- 1365-2435. ; 31:6, s. 1252-1261
  • Journal article (peer-reviewed)abstract
    • Life-history theory predicts a trade-off between early-life fitness and life span. While the focus traditionally has been on the fecundity-life span trade-off, there are strong reasons to expect trade-offs with growth rate and/or development time. We investigated the roles of growth rate and development time in the evolution of life span in two independent selection experiments in the outcrossing nematode Caenorhabditis remanei. First, we found that selection under heat-shock leads to the evolution of increased life span without fecundity costs, but at the cost of slower development. Thereafter, the putative evolutionary links between development time, growth rate, fecundity, heat-shock resistance and life span were independently assessed in the second experiment by directly selecting for fast or slow development. This experiment confirmed our initial findings, since selection for slow development resulted in the evolution of long life span and increased heat-shock resistance. Because there were no consistent trade-offs with growth rate or fecundity, our results highlight the key role of development rate - differentiation of the somatic cells per unit of time - in the evolution of life span. Since development time is under strong selection in nature, reduced somatic maintenance resulting in shorter life span may be a widespread cost of rapid development.
  •  
34.
  • Maklakov, Alexei A., et al. (author)
  • Ageing : Why Males Curtail the Longevity of Their Mates
  • 2016
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 26:20, s. R929-R932
  • Journal article (other academic/artistic)abstract
    • Male nematodes secrete pheromones that accelerate the somatic senescence of potential mates. A new study shows that this harm most likely is an unintended by-product of the males' aim to speed up sexual maturation and delay reproductive senescence of future partners.
  •  
35.
  • Maklakov, Alexei A., et al. (author)
  • Ageing and the evolution of female resistance to remating in seed beetles
  • 2006
  • In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 2:1, s. 62-64
  • Journal article (peer-reviewed)abstract
    • Female remating behaviour is a key mating system parameter that is predicted to evolve according to the net effect of remating on female fitness. In many taxa, females commonly resist male remating attempts because of the costs of mating. Here, we use replicated populations of the seed beetle Acanthoscelides obtectus selected for either early or late life reproduction and show that 'Early' and 'Late' females evolved different age-specific rates of remating. Early females were more likely to remate with control males as they aged, while Late females were more resistant to remating later in life. Thus, female remating rate decreases with age when direct selection on late-life fitness is operating and increases when such selection is relaxed. Our findings not only demonstrate that female resistance to remating can evolve rapidly, but also that such evolution is in accordance with the genetic interests of females.
  •  
36.
  • Maklakov, Alexei A. (author)
  • Aging : Why Do Organisms Live Too Long?
  • 2013
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 23:22, s. R1003-R1005
  • Journal article (other academic/artistic)
  •  
37.
  • Maklakov, Alexei A., et al. (author)
  • Brains and the city : big-brained passerine birds succeed in urban environments
  • 2011
  • In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 7:5, s. 730-732
  • Journal article (peer-reviewed)abstract
    • Urban regions are among the most human-altered environments on Earth and they are poised for rapid expansion following population growth and migration. Identifying the biological traits that determine which species are likely to succeed in urbanized habitats is important for predicting global trends in biodiversity. We provide the first evidence for the intuitive yet untested hypothesis that relative brain size is a key factor predisposing animals to successful establishment in cities. We apply phylogenetic mixed modelling in a Bayesian framework to show that passerine species that succeed in colonizing at least one of 12 European cities are more likely to belong to big-brained lineages than species avoiding these urban areas. These data support findings linking relative brain size with the ability to persist in novel and changing environments in vertebrate populations, and have important implications for our understanding of recent trends in biodiversity.
  •  
38.
  • Maklakov, Alexei A., et al. (author)
  • Brains and the city in passerine birds : re-analysis and confirmation of the original result
  • 2013
  • In: Biology Letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 9:6, s. 20130859-
  • Journal article (peer-reviewed)abstract
    • Our original paper [1] included two Bayesian analyses [2] of the association between brain size and the probability of a passerine species of bird breeding in the city centre—at the level of families and at the level of individual species—with both analyses suggesting the same pattern. It has since been brought to our attention that in one of the analyses at the level of individual species, the residual variance was not fixed to 1 resulting in overestimation of the variance. We re-ran the analysis using fixed residual variance and the results support the original conclusion that relative brain size is associated with breeding in the city centre (ln brain size: posterior mean, 324.53, 95% credibility interval, 52.61–601.35; ln body size: posterior mean, −276.22, 95% credibility interval, −490.60 to −70.32). Furthermore, we applied a complimentary approach using logistic regression to test whether brain size predicts breeding in the city centre (yes/no) without accounting for phylogeny. This analysis also resulted in a significant positive association between brain size and breeding in city centres (likelihood ratio tests: ln brain size: d.f. = 1, χ2 = 11.08, p = 0.0009; ln body size: d.f. = 1, χ2 = 11.26, p = 0.0008). Thus, our results are confirmed by both phylogenetic and non-phylogenetic analyses.
  •  
39.
  • Maklakov, Alexei A., et al. (author)
  • Evolution of sex differences in lifespan and aging : Causes and constraints
  • 2013
  • In: Bioessays. - : Wiley. - 0265-9247 .- 1521-1878. ; 35:8, s. 717-724
  • Journal article (peer-reviewed)abstract
    • Why do the two sexes have different lifespans and rates of aging? Two hypotheses based on asymmetric inheritance of sex chromosomes (unguarded X) or mitochondrial genomes (mother's curse) explain sex differences in lifespan as sex-specific maladaptation leading to increased mortality in the shorter-lived sex. While asymmetric inheritance hypotheses equate long life with high fitness, considerable empirical evidence suggests that sexes resolve the fundamental tradeoff between reproduction and survival differently resulting in sex-specific optima for lifespan. However, selection for sex-specific values in life-history traits is constrained by intersexual genetic correlations resulting in intra-locus sexual conflict over optimal lifespan. The available data suggest that the evolution of sexual dimorphism only partially resolves these conflicts. Sexual conflict over optimal trait values, which has been demonstrated in model organisms and in humans, is likely to play a key role in shaping the evolution of lifespan, as well as in maintaining genetic variation for sex-specific diseases.
  •  
40.
  • Maklakov, Alexei A., et al. (author)
  • Indirect genetic benefits of polyandry in a spider with direct costs of mating
  • 2006
  • In: Behavioral Ecology and Sociobiology. - : Springer Science and Business Media LLC. - 0340-5443 .- 1432-0762. ; 61:1, s. 31-38
  • Journal article (peer-reviewed)abstract
    • The search for the evolutionary explanation of polyandry is increasingly focused on direct and indirect selection on female resistance. In a polyandrous spider Stegodyphus lineatus, males do not provide material benefits and females are resistant to remating. Nevertheless, polyandrous females may obtain indirect genetic benefits that offset the costs associated with multiple mating. We manipulated the opportunity for females to select between different partners and examined the effect of female mating history (mated once, mated twice, or rejected the second male) on offspring body mass, size, condition, and survival under high- and low-food rearing regimens. We found that multiple mating, not female choice, results in increased female offspring body mass and condition. However, these effects were present only in low-food regimen. We did not find any effects of female mating history on male offspring variables. Thus, the benefits of polyandry depend not only on sex, but also on offspring environment. Furthermore, the observed patterns suggest that indirect genetic benefits cannot explain the evolution of female resistance in this system.
  •  
41.
  • Maklakov, Alexei A., et al. (author)
  • Sexual selection affects lifespan and aging in the seed beetle
  • 2007
  • In: Aging Cell. - : Wiley. - 1474-9718 .- 1474-9726. ; 6:6, s. 739-744
  • Journal article (peer-reviewed)abstract
    • Sexual selection in general, and sexual conflict in particular, should affect the evolution of lifespan and aging. Using experimental evolution, we tested whether removal of sexual selection leads to the evolution of accelerated or decelerated senescence. We subjected replicated populations of the seed beetle Callosobruchus maculatus to either of two selection regimes for 35 generations. These regimes either allowed (polygamy) or removed the potential (monogamy) for sexual selection to operate. To test for the evolution of intrinsic differences between the two selection regimes, we assayed longevity in replicate cohorts of virgin females and males. Virgin females from populations evolving under sexual selection had reduced lifespan as predicted by the sexual conflict theory of aging. However, this reduction was due to increased baseline mortality rather than an increase in age-specific mortality rates with age. We discuss these findings in light of other data from this model system and suggest that system-specific idiosyncrasies may often modulate the general effects of male-female coevolution on the evolution of aging.
  •  
42.
  • Maklakov, Alexei A., et al. (author)
  • Sexual selection did not contribute to the evolution of male lifespan under curtailed age at reproduction in a seed beetle
  • 2009
  • In: Ecological Entomology. - : Wiley. - 0307-6946 .- 1365-2311. ; 34:5, s. 638-643
  • Journal article (peer-reviewed)abstract
    • 1. Sexual selection is a powerful evolutionary force that is hypothesised to play an important role in the evolution of lifespan. Here we test for the potential contribution of sexual selection to the rapid evolution of male lifespan in replicated laboratory populations of the seed beetle, Callosobruchus maculatus. 2. For 35 generations, newly hatched virgin male beetles from eight different populations were allowed to mate for 24 h and then discarded. Sexual selection was removed in half of these populations by enforcing random monogamy. 3. Classic theory predicts that because of sexual competition, males from sexually selected lines would have higher age-specific mortality rates and shorter lifespan than males from monogamous lines. 4. Alternatively, condition-dependent sexual selection may also favour genes that have positive pleiotropic effects on lifespan and ageing. 5. Males from all eight populations evolved shorter lifespans compared with the source population. However, there was no difference in lifespan between males from populations with or without sexual selection. Thus, sexual selection did not contribute to the evolution of male lifespan despite the fact that such evolution did occur in our study populations.
  •  
43.
  • Maklakov, Alexei A., et al. (author)
  • Testing for Direct and Indirect Effects of Mate Choice by Manipulating Female Choosiness
  • 2009
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 19:22, s. 1903-1906
  • Journal article (peer-reviewed)abstract
    • Despite a massive research effort, our understanding of the evolution of female mate choice remains incomplete [1, 2]. A central problem is that the predominating empirical research tradition has focused on male traits, yet the key question is whether female choice traits are maintained because of direct effects on female fitness or because of indirect genetic effects in offspring that may be associated with such traits. Here, we address this question by using a novel research strategy that employs experimental phenotypic manipulation of a female choice trait in an insect model system, the seed beetle Callosobruchus chinensis (Coleoptera: Bruchidae). We show that females with increased efficiency of choice enjoy strongly elevated fitness compared to females with reduced choice efficiency. In contrast, we found no effects of female choice efficiency on offspring fitness. Our results show that female choice is maintained by direct selection in females in this system, whereas indirect selection is relatively weak at most. We suggest that phenotypic engineering of female choice traits can greatly advance our ability to elucidate the relative importance of direct and indirect selection for the maintenance of female choice.
  •  
44.
  • Maklakov, Alexei A., et al. (author)
  • The effect of sexual harassment on lethal mutation rate in female Drosophila melanogaster
  • 2013
  • In: Proceedings of the Royal Society of London. Biological Sciences. - London, UK : The Royal Society. - 0962-8452 .- 1471-2954. ; 280:1750, s. 20121874-
  • Journal article (peer-reviewed)abstract
    • The rate by which new mutations are introduced into a population may have far-reaching implications for processes at the population level. Theory assumes that all individuals within a population have the same mutation rate, but this assumption may not be true. Compared with individuals in high condition, those in poor condition may have fewer resources available to invest in DNA repair, resulting in elevated mutation rates. Alternatively, environmentally induced stress can result in increased investment in DNA repair at the expense of reproduction. Here, we directly test whether sexual harassment by males, known to reduce female condition, affects female capacity to alleviate DNA damage in Drosophila melanogaster fruitflies. Female gametes can repair double-strand DNA breaks in sperm, which allows manipulating mutation rate independently from female condition. We show that male harassment strongly not only reduces female fecundity, but also reduces the yield of dominant lethal mutations, supporting the hypothesis that stressed organisms invest relatively more in repair mechanisms. We discuss our results in the light of previous research and suggest that social effects such as density and courtship can play an important and underappreciated role in mediating condition-dependent mutation rate.
  •  
45.
  • Maklakov, Alexei A., et al. (author)
  • The effects of male age at mating on female life-history traits in a seed beetle
  • 2007
  • In: Behavioral Ecology. - : Oxford University Press (OUP). - 1045-2249 .- 1465-7279. ; 18:3, s. 551-555
  • Journal article (peer-reviewed)abstract
    • Age at first reproduction is an important component of life history across taxa and can ultimately affect fitness. Because genetic interests of males and females over reproductive decisions commonly differ, theory predicts that conflict may arise over the temporal distribution of matings. To determine the potential for such sexual conflict, we studied the direct costs and benefits associated with mating at different times for females, using seed beetles (Acanthoscelides obtectus) as a model system. Virgin females were resistant to male mating attempts at a very early age but subsequently reduced their resistance. Although we found no difference in life span or mortality rates between females mated early in life and those mated later, females that mated early in life suffered a 12% reduction in lifetime fecundity. Thus, there are direct costs associated with mating early in life for females. Yet, males mate even with newly hatched females. We suggest that these data indicate a potential for sexual conflict over the timing of first mating and that female resistance to mating, at least in part, may represent a female strategy aimed at delaying mating to a later time in life.
  •  
46.
  • Maklakov, Alexei A., et al. (author)
  • The Expensive Germline and the Evolution of Ageing
  • 2016
  • In: Current Biology. - : Elsevier BV. - 0960-9822 .- 1879-0445. ; 26:13, s. R577-R586
  • Research review (peer-reviewed)abstract
    • The trade-off between survival and reproduction is the bedrock of the evolutionary theory of ageing. The reproductive system regulates ageing of the soma, and removal of germ cells extends somatic lifespan and increases resistance to a broad variety of abiotic and biotic stresses. The general explanation for this somatic response is that reduced reproduction frees up resources for survival. Remarkably, however, the disruption of molecular signaling pathways that regulate ageing increases lifespan without the obligatory reduction in fecundity, thus challenging the key role of the survival-reproduction trade-off. Here, we review the diverse literature on the costs of lifespan extension and suggest that the current paradigm is overly centered on the trade-off between lifespan and fecundity, often neglecting key aspects of fitness, such as development time, defense against parasites and, in particular, the high costs of germline maintenance. Compromised germline maintenance increases germline mutation rate, which reduces offspring fitness and ultimately can terminate germline proliferation across generations. We propose that future work should incorporate the costs of germline maintenance in the study of ageing evolution, as well as in applied biomedical research, by assessing offspring fitness.
  •  
47.
  • Maklakov, Alexei A., et al. (author)
  • The roles of life-history selection and sexual selection in the adaptive evolution of mating behavior in a beetle
  • 2010
  • In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 64:5, s. 1273-1282
  • Journal article (peer-reviewed)abstract
    • Although there is continuing debate about whether sexual selection promotes or impedes adaptation to novel environments, the role of mating behavior in such adaptation remains largely unexplored We investigated the evolution of mating behavior (latency to mating, mating probability and duration) in replicate populations of seed beetles Callosobruchus maculatus subjected to selection on life-history ("Young" vs. "Old" reproduction) under contrasting regimes of sexual selection ("Monogamy" vs. "Polygamy"). Life-history selection is predicted to favor delayed mating in "Old" females, but sexual conflict under polygamy can potentially retard adaptive life-history evolution. We found that life-history selection yielded the predicted changes in mating behavior, but sexual selection regime had no net effect. In within-line crosses, populations selected for late reproduction showed equally reduced early-life mating probability regardless of mating system. In between-line crosses, however, the effect of life-history selection on early-life mating probability was stronger in polygamous lines than in monogamous ones. Thus, although mating system influenced male-female coevolution, removal of sexual selection did not affect the adaptive evolution of mating behavior Importantly, our study shows that the interaction between sexual selection and life-history selection can result in either increased or decreased reproductive divergence depending on the ecological context.
  •  
48.
  • Maklakov, Alexei A., et al. (author)
  • Why organisms age : Evolution of senescence under positive pleiotropy?
  • 2015
  • In: Bioessays. - : Wiley. - 0265-9247 .- 1521-1878. ; 37:7, s. 802-807
  • Journal article (peer-reviewed)abstract
    • Two classic theories maintain that aging evolves either because of alleles whose deleterious effects are confined to late life or because of alleles with broad pleiotropic effects that increase early-life fitness at the expense of late-life fitness. However, empirical studies often reveal positive pleiotropy for fitness across age classes, and recent evidence suggests that selection on early-life fitness can decelerate aging and increase lifespan, thereby casting doubt on the current consensus. Here, we briefly review these data and promote the simple argument that aging can evolve under positive pleiotropy between early-and late-life fitness when the deleterious effect of mutations increases with age. We argue that this hypothesis makes testable predictions and is supported by existing evidence.
  •  
49.
  • Maklakov, Alexei A, et al. (author)
  • Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster
  • 2006
  • In: Evolution. - : Wiley. - 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.
  •  
50.
  • Maklakov, Alexei A., et al. (author)
  • Within-population variation in cytoplasmic genes affects female life span and aging in Drosophila melanogaster
  • 2006
  • 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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