Coevolution of longevity and female germline maintenance.

An often-overlooked aspect of life-history optimization is the allocation of resources to protect the germline and secure safe transmission of genetic information. While failure to do so renders significant fitness consequences in future generations, germline maintenance comes with substantial costs. Thus, germline allocation should trade off with other life-history decisions and be optimized in accordance with an organism's reproductive schedule. Here, we tested this hypothesis by studying germline maintenance in lines of seed beetle, selected for early (E) or late (L) reproduction for 350 and 240 generations, respectively. Female animals provide maintenance and screening of male gametes in their reproductive tract and oocytes. Here, we reveal the ability of young and aged E- and L-females to provide this form of germline maintenance by mating them to males with ejaculates with artificially elevated levels of protein and DNA damage. We find that germline maintenance in E-females peaks at young age and then declines, while the opposite is true for L-females, in accordance with the age of reproduction in the respective regime. These findings identify the central role of allocation to secure germline integrity in life-history evolution and highlight how females can play a crucial role in mitigating the effects of male germline decisions on mutation rate and offspring quality.

Experimental Life History Evolution Results in Sex-specific Evolution of Gene Expression in Seed Beetles.

The patterns of reproductive timing and senescence vary within and across species owing to differences in reproductive strategies, but our understanding of the molecular underpinnings of such variation is incomplete. This is perhaps particularly true for sex differences. We investigated the evolution of sex-specific gene expression associated with life history divergence in replicated populations of the seed beetle Acanthoscelides obtectus, experimentally evolving under (E)arly or (L)ate life reproduction for >200 generations which has resulted in strongly divergent life histories. We detected 1,646 genes that were differentially expressed in E and L lines, consistent with a highly polygenic basis of life history evolution. Only 30% of differentially expressed genes were similarly affected in males and females. The evolution of long life was associated with significantly reduced sex differences in expression, especially in non-reproductive tissues. The expression differences were overall more pronounced in females, in accordance with their greater phenotypic divergence in lifespan. Functional enrichment analysis revealed differences between E and L beetles in gene categories previously implicated in aging, such as mitochondrial function and defense response. The results show that divergent life history evolution can be associated with profound changes in gene expression that alter the transcriptome in a sex-specific way, highlighting the importance of understanding the mechanisms of aging in each sex.

Sexual Dimorphism and Morphological Modularity in Acanthoscelides obtectus (Say, 1831) (Coleoptera: Chrysomelidae): A Geometric Morphometric Approach.

Sexual dimorphism and specific patterns of development contribute in a great manner to the direction and degree of the sexual differences in body size and shape in many insects. Using a landmark-based geometric morpohometrics approach, we investigated sex-specific morphological size and shape variation in the seed beetle, Acanthoscelides obtectus. We also tested the functional hypothesis of the two morphological modules-thorax and abdomen in both sexes. Female-biased sexual dimorphism in size was shown, while differences in shape were reflected in the wider thorax and abdomen and shorter abdomen in females in comparison to males. The functional hypothesis of a two-module body was confirmed only in females before correction for size, and in both sexes after the allometry correction. Our results indicate that reproductive function has the central role in forming the patterns of modularity. We hypothesize that high morphological integration of the abdomen in females results from intense stabilizing selection, while the more relaxed integration in males is driven by the higher intensity of sexual selection.

Potential for Acanthoscelides obtectus to Adapt to New Hosts Seen in Laboratory Selection Experiments.

Effective pest management strategies for a targeted pest species must rely on accurate, reliable and reproducible estimates of population dynamics. Importance of such approaches is even more conspicuous when assessing pest's potential to utilize other stored products. Using an experimental evolution approach, we have focused our attention on a common bean pest, the seed beetle (Acanthoscelides obtectus). We looked into the potential to invade and sustain population growth on two suboptimal host plants (chickpeas and mung beans). Such an approach simulates steps of the host-shift process in storages. By analyzing population dynamics during initial encountering with a new host plant, we detected a population drop for both novel hosts. However, transgenerational development in a novel environment resulted in a constant population growth in chickpeas, but not in mung bean populations. Reversal of chickpea selected populations to original host plant has led to a severe decrease in population parameters due to low viability of immatures, while the opposite trend was detected in mung bean populations. This paper highlights the importance of good practice in estimating population dynamics for economically important species. With special emphasis on storage pest species, we discuss how this approach can be useful for estimating invading potential of pest insects.

The consequences of sexual selection in well-adapted and maladapted populations of bean beetles†.

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modeling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex-specific strengths of selection and IaSC by cross-rearing the two experimental evolution regimes on the alternative hosts and estimating within-population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male-bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.

Divergent evolution of life span associated with mitochondrial DNA evolution.

Mitochondria play a key role in ageing. The pursuit of genes that regulate variation in life span and ageing have shown that several nuclear-encoded mitochondrial genes are important. However, the role of mitochondrial encoded genes (mtDNA) is more controversial and our appreciation of the role of mtDNA for the evolution of life span is limited. We use replicated lines of seed beetles that have been artificially selected for long or short life for >190 generations, now showing dramatic phenotypic differences, to test for a possible role of mtDNA in the divergent evolution of ageing and life span. We show that these divergent selection regimes led to the evolution of significantly different mtDNA haplotype frequencies. Selection for a long life and late reproduction generated positive selection for one specific haplotype, which was fixed in most such lines. In contrast, selection for reproduction early in life led to both positive selection as well as negative frequency-dependent selection on two different haplotypes, which were both present in all such lines. Our findings suggest that the evolution of life span was in part mediated by mtDNA, providing support for the emerging general tenet that adaptive evolution of life-history syndromes may involve mtDNA.

Sex-specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics, ageing, and life history in seed beetles.

The role of mitochondrial DNA for the evolution of life-history traits remains debated. We examined mitonuclear effects on the activity of the multisubunit complex of the electron transport chain (ETC) involved in oxidative phosphorylation (OXPHOS) across lines of the seed beetle Acanthoscelides obtectus selected for a short (E) or a long (L) life for more than >160 generations. We constructed and phenotyped mitonuclear introgression lines, which allowed us to assess the independent effects of the evolutionary history of the nuclear and the mitochondrial genome. The nuclear genome was responsible for the largest share of divergence seen in ageing. However, the mitochondrial genome also had sizeable effects, which were sex-specific and expressed primarily as epistatic interactions with the nuclear genome. The effects of mitonuclear disruption were largely consistent with mitonuclear coadaptation. Variation in ETC activity explained a large proportion of variance in ageing and life-history traits and this multivariate relationship differed somewhat between the sexes. In conclusion, mitonuclear epistasis has played an important role in the laboratory evolution of ETC complex activity, ageing, and life histories and these are closely associated. The mitonuclear architecture of evolved differences in life-history traits and mitochondrial bioenergetics was sex-specific.

Experimentally induced host-shift changes life-history strategy in a seed beetle.

Expansion of the host range in phytophagous insects depends on their ability to form an association with a novel plant through changes in host-related traits. Phenotypic plasticity has important effects on initial survival of individuals faced with a new plant, as well as on the courses of evolutionary change during long-term adaptation to novel conditions. Using experimental populations of the seed beetle that evolved on ancestral (common bean) or novel (chickpea) host and applying reciprocal transplant at both larval and adult stage on the alternative host plant, we studied the relationship between the initial (plastic) phases of host-shift and the subsequent stages of evolutionary divergence in life-history strategies between populations exposed to the host-shift process. After 48 generations, populations became well adapted to chickpea by evolving the life-history strategy with prolonged larval development, increased body mass, earlier reproduction, shorter lifespan and decreased plasticity of all traits compared with ancestral conditions. In chickpea-adapted beetles, negative fitness consequences of low plasticity of pre-adult development (revealed as severe decrease in egg-to-adult viability on beans) exhibited mismatch with positive effects of low plasticity (i.e. low host sensitivity) in oviposition and fecundity. In contrast, beetles adapted to the ancestral host showed high plasticity of developmental process, which enabled high larval survival on chickpea, whereas elevated plasticity in adult behaviour (i.e. high host sensitivity) resulted in delayed reproduction and decreased fecundity on chickpea. The analysis of population growth parameters revealed significant fluctuation during successive phases of the host-shift process in A. obtectus.

Heterosis in age-specific selected populations of a seed beetle: sex differences in longevity and reproductive behavior.

We tested mutation accumulation hypothesis for the evolution of senescence using short-lived and long-lived populations of the seed-feeding beetle, Acanthoscelides obtectus (Say), obtained by selection on early- and late-life for many generations. The expected consequence of the mutation accumulation hypothesis is that in short-lived populations, where the force of natural selection is the strongest early in life, the late-life fitness traits should decline due to genetic drift which increases the frequency of mutations with deleterious effects in later adult stages. Since it is unlikely that identical deleterious mutations will increase in several independent populations, hybrid vigor for late-life fitness is expected in offspring obtained in crosses among populations selected for early-life fitness traits. We tested longevity of both sexes, female fecundity and male reproductive behavior for hybrid vigor by comparing hybrid and nonhybrid short-lived populations. Hybrid vigor was confirmed for male virility, mating speed and copulation duration, and longevity of both sexes at late ages. In contrast to males, the results on female fecundity in short-lived populations did not support mutation accumulation as a genetic mechanism for the evolution of this trait. Contrary to the prediction of this hypothesis, male mating ability indices and female fecundity in long-lived populations exhibited hybrid vigor at all assayed age classes. We demonstrate that nonhybrid long-lived populations diverged randomly regarding female and male reproductive fitness, indicating that sexually antagonistic selection, when accompanied with genetic drift for female fecundity and male virility, might be responsible for overriding natural selection in the independently evolving long-lived populations.

The effect of mitochondrial complex I inhibitor on longevity of short-lived and long-lived seed beetles and its mitonuclear hybrids.

Mitochondria are suggested to play a central role in ageing and evolution of longevity. Gradual decline in mitochondrial function during ageing and concomitant increase in production of reactive oxygen species (ROS) leads to oxidative damage of macromolecules and impairment of ATP synthesis. To assess relationship between ageing and oxidative stress resistance we exposed different longevity lines of the seed beetle (Acanthoscelides obtectus) to four concentrations of tebufenpyrad, mitochondrial complex I inhibitor. Complex I is one of main sites of ROS production during normal respiration and its inhibition elevates oxidative stress. Our results showed that 24 h of exposure to tebufenpyrad decreased survival and post-stress longevity due to increased baseline mortality. Higher resistance was recorded in beetles from lines selected for late reproduction and extended longevity (L) than in early reproducing beetles (E). Also, females were more resistant than males. Since complex I is under dual genetic control, our second aim was to disentangle relative contribution of nuclear and mitochondrial genes to the variation in longevity. We used crossed combinations of distinct mitochondrial and nuclear genotypes (E × L, L × E) and compared them to control hybrids where mitochondrial genome was "transplanted" onto the original background (E × E, L × L). Our study revealed significant effect of nucleus, i.e. higher survival and post-stress longevity in beetles harbouring L nucleus. Mitochondrion effect was significant only within L nuclear background where E mitochondrion gave advantage.