Biljana Stojković

Homosexual behaviour and its longevity cost in females and males of the seed beetle Acanthoscelides obtectus

The level of homosexual behaviour is evaluated in one laboratory population of seed beetle and derived lines selected to reproduce early (E) or late in life (L), where inadvertent selection for either low or high heterosexual activity has been detected. The magnitudes of homosexual interaction, measured as chasing and mounting individuals of the same sex, are estimated over different age classes. These magnitudes are correlated with previously observed levels and patterns of age‐specific variation of heterosexual activity of both sexes in the E and L experimental lines. The results obtained support the perception error hypothesis proposing that a low degree of sexual discrimination is genetically correlated with high sexual activity. The fitness costs of the same‐sex interactions are tested by assessing their effects on longevity. In both sexes, the longevities of homosexual pairs are reduced relative to individually‐housed virgin beetles in both the E and L lines, although homosexual interactions have a more pronounced effect on male survival than on female survival. Although the results obtained suggest that the longevity cost of homosexual interactions can be substantial, this cost is much smaller than the cost of heterosexual interactions.

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.

Resistance to prooxidant agent paraquat in the short- and long-lived lines of the seed beetle (Acanthoscelides obtectus)

In the present study we test whether variation in resistance to paraquat (PQ), a free radical generator, correlates with variation in longevity in two sets of seed beetles (Acanthoscelides obtectus) experimental lines that were selected either for early reproduction and short-life or late reproduction and long-life. Long-lived late reproduction lines (L) showed increased resistance to PQ, while opposite was true for short-lived early reproduction line (E). Striking outcome of the selection for early and late reproduction in A. obtectus is asymmetry of responses to alternate mating schedules. The intensity of response depended on selection regime, sex and PQ dose. Evolution of longevity and PQ resistance was faster in L than E selection regime, and in females than males. To understand how age-specific mortality rates are affected by PQ we decomposed post-stress mortality data (using Gompertz mortality model) into initial mortality rate, which reflects basal vulnerability to stresses and age-specific mortality rate, which concerns the rate of increase in stress vulnerability, i.e. the rate of senescence. By estimating the parameters of the Gompertz mortality model we have shown that longevity reduction caused by PQ was the consequence of the increased baseline mortality rather than a speed up of the rate of ageing.

The consequences of sexual selection in well-adapted and amaladapted populations of bean beetles : Sexual selection in maladapted populations

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.

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.

Intergenomic Interactions in Hybrids Between Short-Lived and Long-Lived Lines of a Seed Beetle: Analyses of Life History Traits

Products and regulatory motifs of the mitochondrial and nuclear genomes interact closely to enable efficient cellular energy production within mitochondria. Although recent evidences support the prediction that during evolutionary time combinations of these interactions are optimized by selection acting on important life history traits, relatively few studies have directly tested it. The goal of this study was to test the role of mitonuclear interactions in shaping preadult and adult life history traits under age-specific selection in the seed beetle (Acanthoscelides obtectus). In order to disentangle the effects of mitochondria, nuclei and their interaction in the evolutionary response to the long-term laboratory selection for early (E) and late (L) reproduction, we used mitonuclear introgression lines in which E and L mitochondrial genomes were expressed in both E and L nuclear background. We found that mitonuclear genotypes carrying disrupted pair of nuclear and mitochondrial genomes mainly affected preadult life history traits—egg-to-adult viability and developmental time. Neither mitochondria nor their interaction with nuclear genomes had effects on realized fecundity of mated females and longevity of virgin beetles. However, when involved in reproductive activities females and males with disrupted genotypes mostly exhibited reduced longevity. Furthermore, since reproduced males exhibited greater longevity cost than females, our results are in accordance with the mother’s curse hypothesis. Being that for the most life history traits we detected smaller additive mitochondrial genetic effects compared with epistatic mitonuclear effects, we concluded that mitonuclear interactions might be the target of age-specific selection.

Adaptive phenotypic plasticity of gypsy moth digestive enzymes

The adaptiveness of plasticity of digestive enzyme responses to allelochemical stress was tested on 32 full-sib families of gypsy moth larvae from an oak forest population (the Quercus population) and 26 families from a locust-tree forest (the Robinia population), reared either on control diet, or on tannin-supplemented diet. Using the duration of larval development as an indirect measure of fitness, phenotypic selection analyses revealed that lower specific activities of total proteases and trypsin, and higher specific activity of leucine aminopeptidase were adaptive for both populations in the control environment. Plasticity was only shown to be costly for total proteases and trypsin activity in Quercus larvae. In a stressful environment, the most apparent adaptive response was a significant increase in lipase activity. There was no plasticity cost for lipase activity. The two populations differed in the direction of selection acting on α-glucosidase activity, which favoured decreased activity in Quercus larvae and increased activity in Robinia larvae in the control environment. α-glucosidase activity in Quercus larvae is characterized by cost of homeostasis, while cost of plasticity was shown for Robinia larvae. The results obtained on the plasticity of digestive enzyme activity indicate how this generalist species copes with variation in plant allelochemicals.

The pace-of-life: A sex-specific link between metabolic rate and life history in bean beetles

Metabolic rate (MR) is a key functional trait simply because metabolism converts resources into population growth rate. Yet, our empirical understanding of the sources of within species variation i ...

Host-associated divergence in the activity of digestive enzymes in two populations of the gypsy moth Lymantria dispar (Lepidoptera: Erebidae): Population divergence in the gypsy moth

The gypsy moth is a generalist insect pest with an extremely wide host range. Adaptive responses of digestive enzymes are important for the successful utilization of plant hosts that differ in the contents and ratios of constituent nutrients and allelochemicals. In the present study, we examined the responses of α‐amylase, trypsin, and leucine aminopeptidase to two tree hosts (suitable oak, Quercus cerris, and unsuitable locust tree, Robinia pseudoacacia) in the fourth, fifth, and sixth instars of gypsy moth larvae originating from oak and locust tree forest populations (hereafter assigned as Quercus and Robinia populations, respectively). Gypsy moths from the Robinia forest had been adapting to this unsuitable host for more than 40 generations. To test for population‐level host plant specialization, we applied a two‐population × two‐host experimental design. We compared the levels, developmental patterns, and plasticities of the activities of enzymes. The locust tree diet increased enzyme activity in the fourth instar and reduced activity in advanced instars of the Quercus larvae in comparison to the oak diet. These larvae also exhibited opposite developmental trajectories on the two hosts, i.e. activity increased on the oak diet and decreased on the locust tree diet with the progress of instar. Larvae of the Robinia population were characterized by reduced plasticity of enzyme activity and its developmental trajectories. In addition, elevated trypsin activity in response to an unsuitable host was observed in all instar larvae of the Robinia population, which demonstrated that Robinia larvae had an improved digestive performance than did Quercus larvae.