scholarly journals Sexes suffer from suboptimal lifespan because of genetic conflict in a seed beetle

2012 ◽  
Vol 279 (1745) ◽  
pp. 4296-4302 ◽  
Author(s):  
Elena C. Berg ◽  
Alexei A. Maklakov

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.

2015 ◽  
Author(s):  
Nicola J Barson ◽  
Tutku Aykanat ◽  
Kjetil Hindar ◽  
Matthew Baranski ◽  
Geir H Bolstad ◽  
...  

Males and females share many traits that have a common genetic basis, however selection on these traits often differs between the sexes leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific genetic loci behind sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here, we identify a large effect locus controlling age at maturity in 57 salmon populations, an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex dependent dominance reducing intralocus sexual conflict and maintaining adaptive variation in wild populations. Using high density SNP data and whole genome re-sequencing, we found that vestigial-like family member 3 (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39.4% of phenotypic variation, an unexpectedly high effect size for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal permitting greater optimisation of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We further anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed


Insects ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 310
Author(s):  
Dariusz Krzysztof Małek ◽  
Marcin Czarnoleski

The thermal environment influences insect performance, but the factors affecting insect thermal preferences are rarely studied. We studied Callosobruchus maculatus seed beetles and hypothesized that thermal preferences are influenced by water balance, with individuals with limited water reserves preferring cooler habitats to reduce evaporative water loss. Adult C. maculatus, in their flightless morph, do not consume food or water, but a copulating male provides a female with a nuptial gift of ejaculate containing nutrients and water. We hypothesized that gift recipients would prefer warmer habitats than gift donors and that both sexes would plastically adjust their thermal preferences according to the size of the transferred gift. We measured the thermal preference in each sex in individuals that were mated once or were unmated. In the mated group, we measured the sizes of the nuptial gifts and calculated proportional body mass changes in each mate during copulation. Supporting the role of water balance in thermal preference, females preferred warmer habitats than males. Nevertheless, thermal preferences in either sex were not affected by mating status or gift size. It is likely that high rates of mating and gift transfers in C. maculatus living under natural conditions promoted the evolution of constitutive sex-dependent thermal preferences.


2019 ◽  
Author(s):  
Gao Ke ◽  
Michiel van Wijk ◽  
Zoe Clement ◽  
Martijn Egas ◽  
Astrid Groot

Abstract Background Ever since Darwin, evolutionary biologists have studied sexual selection driving differences in appearance and behaviour between males and females. An unchallenged paradigm in such studies is that one sex (usually the male) signals its quality as a mate to the other sex (usually the female), who is choosy in accepting a partner. Here, we argue that in polygamous species these roles may change dynamically with the mating status of males and females, depending on direct reproductive costs and benefits of multiple matings, and on sperm competition. We test this hypothesis using a polygamous moth species, as in moths not males but females are the signalers and males are the responders. Results We found that multiple matings are beneficial as well as costly for both sexes. Specifically, the number of matings did not affect the longevity of males or females, but when paired with a new virgin mate every night for five nights, only 67% of the males and 14% of the females mated successfully in all five nights. The female’s reproductive output increased with multiple matings, although when paired with a new virgin male every night, additional matings beyond 3 decreased her reproductive output, so that the Bateman gradient for females fit a quadratic model better than a linear model. The male’s reproductive success was positively affected by the number of matings and a linear regression line best fit the data. Simulations of the effect of sperm competition showed that increasing last-male paternity increases the steepness of the male Bateman gradient and thus the male’s relative fitness gain from additional mating. Irrespective of last-male paternity value, the female Bateman gradient is steeper than the male one for up to three matings. Conclusion Our results suggest that choosiness in moths may well change throughout the mating season, with males being more choosy early in the season and females being more choosy after having mated at least three times. This life-history perspective on the costs and benefits of multiple matings for both sexes sheds new light on sexual selection forces acting on sexual signals and responses.


2019 ◽  
Author(s):  
Jessica K. Abbott ◽  
Oscar Rios-Cardenas ◽  
Molly Morris

AbstractAlternative reproductive tactics occur when individuals of the same sex have a suite of morphological and/or behavioural traits that allow them to pursue different reproductive strategies. A common pattern is e.g. the existence of “courter” and “sneaker” tactics within males. We have previously argued that alternative reproductive tactics should be subject to genetic conflict over the phenotypic expression of traits, similar to sexual antagonism. In this process, which we called intra-locus tactical conflict, genetically determined tactics experience conflicting selection on a shared phenotypic trait, such as body size, but a positive genetic correlation between tactics in body size prevents either tactic from reaching its optimum. Recently, other authors have attempted to extend this idea to developmentally plastic alternative reproductive tactics, with mixed results. However, it is not clear whether we should expect intra-locus tactical conflict in developmentally plastic tactics or not. We have therefore run a series of simulation models investigating under what conditions we should expect to see positive estimates of the inter-tactical genetic correlation, since a positive genetic correlation is a prerequisite for the existence of intra-locus tactical conflict. We found that for autosomal, X-linked, and Y-linked genetically-determined tactics, estimated inter-tactical genetic correlations were generally high. However, for developmentally plastic tactics, the genetic correlation depends on the properties of the switching threshold between tactics. If it is fixed, then estimated genetic correlations are positive, but if there is genetic variation in the switch-point, then any sign and magnitude of estimated genetic correlation is possible, even for highly heritable traits where the true underlying correlation is perfect. This means that caution should be used when investigating genetic constraints in plastic phenotypes.


2020 ◽  
Vol 16 (11) ◽  
pp. 20200648
Author(s):  
Nathan W. Anderson ◽  
Carl E. Hjelmen ◽  
Heath Blackmon

Chromosome fusion and fission are primary mechanisms of karyotype evolution. In particular, the fusion of a sex chromosome and an autosome has been proposed as a mechanism to resolve intralocus sexual antagonism. If sexual antagonism is common throughout the genome, we should expect to see an excess of fusions that join sex chromosomes and autosomes. Here, we present a null model that provides the probability of a sex chromosome autosome fusion, assuming all chromosomes have an equal probability of being involved in a fusion. This closed-form expression is applicable to both male and female heterogametic sex chromosome systems and can accommodate unequal proportions of fusions originating in males and females. We find that over 25% of all chromosomal fusions are expected to join a sex chromosome and an autosome whenever the diploid autosome count is fewer than 16, regardless of the sex chromosome system. We also demonstrate the utility of our model by analysing two contrasting empirical datasets: one from Drosophila and one from the jumping spider genus Habronattus . We find that in the case of Habronattus , there is a significant excess of sex chromosome autosome fusions but that in Drosophila there are far fewer sex chromosome autosome fusions than would be expected under our null model.


2018 ◽  
Vol 285 (1878) ◽  
pp. 20180652 ◽  
Author(s):  
Jan-Åke Nilsson ◽  
Andreas Nord

The maximum work rate of animals has recently been suggested to be determined by the rate at which excess metabolic heat generated during work can be dissipated (heat dissipation limitation (HDL) theory). As a first step towards testing this theory in wild animals, we experimentally manipulated brood size in breeding marsh tits ( Poecile palustris ) to change their work rate. Parents feeding nestlings generally operated at above-normal body temperatures. Body temperature in both males and females increased with maximum ambient temperature and with manipulated work rate, sometimes even exceeding 45°C, which is close to suggested lethal levels for birds. Such high body temperatures have previously only been described for birds living in hot and arid regions. Thus, reproductive effort in marsh tits may potentially be limited by the rate of heat dissipation. Females had lower body temperatures, a possible consequence of their brood patch serving as a thermal window facilitating heat dissipation. Because increasing body temperatures are connected to somatic costs, we suggest that the HDL theory may constitute a possible mediator of the trade-off between current and future reproduction. It follows that globally increasing, more stochastic, ambient temperatures may restrict the capacity for sustained work of animals in the future.


2020 ◽  
Vol 49 (4) ◽  
pp. 938-946
Author(s):  
Frank J Messina ◽  
Alexandra M Lish ◽  
Amy Springer ◽  
Zachariah Gompert

Abstract The ability to adapt to a novel host plant may vary among insect populations with different genetic histories, and colonization of a marginal host may be facilitated by genetic admixture of disparate populations. We assembled populations of the seed beetle, Callosobruchus maculatus (F.), from four continents, and compared their ability to infest two hosts, lentil and pea. We also formed two cross-continent hybrids (Africa × N.A. and Africa × S.A.). In pre-selection assays, survival was only ~3% in lentil and ~40% in pea. For three replicate populations per line, colonization success on lentil was measured as cumulative exit holes after 75–175 d. On pea, we estimated the change in larval survival after five generations of selection. Females in all lines laid few eggs on lentil, and survival of F1 larvae was uniformly <5%. Subsequently, however, the lines diverged considerably in population growth. Performance on lentil was highest in the Africa × N.A. hybrid, which produced far more adults (mean > 11,000) than either parental line. At the other extreme, Asian populations on lentil appeared to have gone extinct. The Africa × N.A. line also exhibited the highest survival on pea, and again performed better than either parent line. However, no line displayed a rapid increase in survival on pea, as is sometimes observed on lentil. Our results demonstrate that geographic populations can vary substantially in their responses to the same novel resource. In addition, genetic admixtures (potentially caused by long-distance transport of infested seeds) may facilitate colonization of an initially poor host.


2019 ◽  
Vol 286 (1910) ◽  
pp. 20191664 ◽  
Author(s):  
Elena C. Berg ◽  
Martin I. Lind ◽  
Shannon Monahan ◽  
Sophie Bricout ◽  
Alexei A. Maklakov

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.


Behaviour ◽  
1985 ◽  
Vol 94 (1-2) ◽  
pp. 1-39 ◽  
Author(s):  
Judy Stamps ◽  
Anne Clark ◽  
Pat Arrowood ◽  
Barbara Kus

AbstractDespite widespread theoretical interest in genetic conflict between parents and offspring, there is little empirical evidence that it exists in nature. Theoretical models suggest two outcomes of conflict not predicted by alternate theories: (1) offspring that control the allocation of parental investment might show escalated demand behaviours (e.g., begging) and demand more resources than they could efficiently use and (2) parents might evolve behavioural counterstrategies which prevented offspring from obtaining extra resources, but which were more costly than a "laissez-faire" parental strategy allowing offspring control. These predictions were tested in budgerigars, (Melopsittacus undulatus) in large flight cages at Davis, California. Budgerigar clutches hatch extremely asynchronously, yet all nestlings grew at similar rates and fledged at similar sizes and ages. This independence of hatch order and performance seemed due primarily to the mother budgerigar's allofeeding strategy: females allofed offspring mainly on the basis of size, and only secondarily attended to begging rate. Offspring of a given age and size were treated the same by their mothers regardless of hatch order, and offspring undersized for their age were fed as if they were younger. In contrast, male budgerigars attended to offspring begging rates. Males tended to initiate feeding bouts when offspring begged, and to allofeed vigorous beggers more often. Variance in male allofeeding behaviour allowed comparisons of size-matched families in which females performed nearly all of the allofeeds to nestlings (= female-fed families) with families in which males and females both allofed nestlings (= male-aided families). The parent controlled the allocation of food in female-fed families, while offspring had greater control over food allocation in male-fed families. As was predicted by conflict theory, the female counterstrategy was effective but potentially costly: the food delivery rate of females was only half as fast as males'. Conversely, offspring control resulted in an escalation of beg rate for the same degree of need (as measured by size and growth), and male-aided offspring obtained nearly three times more regurgitations than female-fed nestlings, yet grew at comparable rates and fledged at comparable sizes and ages. Hence, offspring demanded and obtained more food than they could effectively use. Other avian parents also seem to use effective but potentially costly counterstrategies, and other avian offspring may demand more food than they require. Even if initial hatch asynchronies functioned in brood reduction, the parental strategies described here would allow parents to retain control over the timing and conditions for offspring loss.


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