Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

Conservative and compensatory evolution in oxidative phosphorylation complexes of angiosperms with highly divergent rates of mitochondrial genome evolution

Interactions between nuclear and mitochondrial gene products are critical for eukaryotic cell function. Nuclear genes encoding mitochondrial‐targeted proteins (N‐mt genes) experience elevated rates of evolution, which has often been interpreted as evidence of nuclear compensation in response to elevated mitochondrial mutation rates. However, N‐mt genes may be under relaxed functional constraints, which could also explain observed increases in their evolutionary rate. To disentangle these hypotheses, we examined patterns of sequence and structural evolution in nuclear‐ and mitochondrial‐encoded oxidative phosphorylation proteins from species in the angiosperm genus Silene with vastly different mitochondrial mutation rates. We found correlated increases in N‐mt gene evolution in species with fast‐evolving mitochondrial DNA. Structural modeling revealed an overrepresentation of N‐mt substitutions at positions that directly contact mutated residues in mitochondrial‐encoded proteins, despite overall patterns of conservative structural evolution. These findings support the hypothesis that selection for compensatory changes in response to mitochondrial mutations contributes to the elevated rate of evolution in N‐mt genes. We discuss these results in light of theories implicating mitochondrial mutation rates and mitonuclear coevolution as drivers of speciation and suggest comparative and experimental approaches that could take advantage of heterogeneity in rates of mtDNA evolution across eukaryotes to evaluate such theories.     

Within‐population genetic effects of mtDNA on metabolic rate in Drosophila subobscura

A growing body of research supports the view that within‐species sequence variation in the mitochondrial genome (mtDNA) is functional, in the sense that it has important phenotypic effects. However, most of this empirical foundation is based on comparisons across populations, and few studies have addressed the functional significance of mtDNA polymorphism within populations. Here, using mitonuclear introgression lines, we assess differences in whole‐organism metabolic rate of adult Drosophila subobscura fruit flies carrying either of three different sympatric mtDNA haplotypes. We document sizeable, up to 20%, differences in metabolic rate across these mtDNA haplotypes. Further, these mtDNA effects are to some extent sex specific. We found no significant nuclear or mitonuclear genetic effects on metabolic rate, consistent with a low degree of linkage disequilibrium between mitochondrial and nuclear genes within populations. The fact that mtDNA haplotype variation within a natural population affects metabolic rate, which is a key physiological trait with important effects on life‐history traits, adds weight to the emergent view that mtDNA haplotype variation is under natural selection and it revitalizes the question as to what processes act to maintain functional mtDNA polymorphism within populations.     

Evolution of male age‐specific reproduction under differential risks and causes of death: males pay the cost of high female fitness

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.     

SEX DIFFERENCES, SEXUAL SELECTION, AND AGEING: AN EXPERIMENTAL EVOLUTION APPROACH

Life-history (LH) theory predicts that selection will optimize the trade-off between reproduction and somatic maintenance. Reproductive ageing and finite life span are direct consequences of such optimization. Sexual selection and conflict profoundly affect the reproductive strategies of the sexes and thus can play an important role in the evolution of life span and ageing. In theory, sexual selection can favor the evolution of either faster or slower ageing, but the evidence is equivocal. We used a novel selection experiment to investigate the potential of sexual selection to influence the adaptive evolution of age-specific LH traits. We selected replicate populations of the seed beetle Callosobruchus maculatus for age at reproduction ("Young" and "Old") either with or without sexual selection. We found that LH selection resulted in the evolution of age-specific reproduction and mortality but these changes were largely unaffected by sexual selection. Sexual selection depressed net reproductive performance and failed to promote adaptation. Nonetheless, the evolution of several traits differed between males and females. These data challenge the importance of current sexual selection in promoting rapid adaptation to environmental change but support the hypothesis that sex differences in LH—a historical signature of sexual selection—are key in shaping trait responses to novel selection.     

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.     

Episodes of adaptive evolution of mitochondrial genome in asiatic salamanders (Amphibia,Caudata, Hynobiidae)

To elucidate the effect of natural selection on the evolution of mitochondrial DNA (mtDNA) in Asiatic salamanders of the family Hynobiidae, nucleotide sequences of 12 protein-coding genes were analyzed. Using a mixed effects model of evolution, it was found that, in spite of the pronounced effect of negative selection on the mtDNA evolution in Hynobiidae (which is typical for the animals in general), two phylogenetic clusters, the West Asian one, represented by the genera Ranodon and Paradactylodon, and North Eurasian one, represented by the genus Salamandrella, were formed under the influence of episodic positive selection. Analysis of protein sequences encoded by the mitochondrial genome also supported the influence of positive selection on the evolution of Hynobiidae at some stages of their cladogenesis. It is suggested that the signatures of adaptive evolution detected in the mtDNA of Hynobiidae were determined by the complex and long-lasting history of their formation, accompanied by adaptation to the changing environment.     

Sexual selection did not contribute to the evolution of male lifespan under curtailed age at reproduction in a seed beetle

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.     

The maintenance of mitochondrial genetic variation by negative frequency‐dependent selection

Mitochondrial genes generally show high levels of standing genetic variation, which is puzzling given the accumulating evidence for phenotypic effects of mitochondrial genetic variation. Negative frequency‐dependent selection, where the relative fitness of a genotype is inversely related to its frequency in a population, provides a potent and potentially general process that can maintain mitochondrial polymorphism. We assessed the change in mitochondrial haplotype frequencies over 10 generations of experimental evolution in 180 seed beetle populations in the laboratory, where haplotypes competed for propagation to subsequent generations. We found that haplotypes consistently increased in frequency when they were initially rare and decreased in frequency when initially common. Our results have important implications for the use of mtDNA haplotype frequency data to infer population level processes and they revive the general hypothesis that negative frequency‐dependent selection, presumably caused by habitat heterogeneity, may commonly promote polymorphism in ecologically relevant life history genes.     

Natural selection and the evolution of mtDNA-encoded peptides: evidence for intergenomic co-adaptation.

Mitochondrial DNA (mtDNA) variation is an important tool for the investigation of the population genetics of animal species. Recently, recognition of the role of mtDNA mutations in human disease has spurred increasing interest in the function and evolution of mtDNA and the 13 polypeptides it encodes. These proteins interact with a large number of peptides encoded in the nucleus to form the mitochondrial electron transport system (ETS). As the ETS is the primary energy generation system in aerobic metazoans, natural selection would be expected to favor mutations that enhance ETS function. Such mutations could occur in either the mitochondrial or nuclear genes encoding ETS proteins and would lead to positive intergenomic interactions, or co-adaptation. Direct evidence for intergenomic co-adaptation comes from functional studies of systems where nuclear-mitochondrial DNA combinations vary naturally or can be manipulated experimentally.     

Molecular Evolution of Cytochrome c Oxidase in High-Performance Fish (Teleostei: Scombroidei)

The 13 peptides encoded by vertebrate mitochondrial DNA (mtDNA) are essential subunits of oxidative phosphorylation (OXPHOS) enzymes. These genes normally experience purifying selection and also coevolve with nuclear-encoded subunits of OXPHOS complexes. However, the role of positive selection on mtDNA evolution is still unclear, as most examples of intergenomic coevolution appear to be the result of compensation by nuclear-encoded genes for mildly deleterious mtDNA mutations, and not simultaneous positive selection in both genomes. Organisms that have experienced strong selective pressures to increase aerobic capacity or adapt to changes in thermal environment may be better candidates in which to examine the impact of positively selected changes on mtDNA evolution. The tuna (suborder Scombroidei, family Scombridae) and billfish (suborder Scombroidei, families Xiphiidae and Istiophoridae) are highly aerobic fish with multiple specializations in muscle energetics, including a high mitochondrial content and regional endothermy. We examined the role of positively selected mtDNA substitutions in the production of these unique phenotypes. Focusing on a catalytic subunit of cytochrome c oxidase (COX II), we found that the rate ratio of nonsynonymous (d(N); amino acid changing)-to-synonymous (d(S); silent) substitutions was not increased in lineages leading to the tuna but was significantly increased in the lineage preceding the billfish. Furthermore, there are a number of individual positively selected sites that, when mapped onto the COX crystal structure, appear to interact with other COX subunits and may affect OXPHOS function and regulation in billfish.     

Multivariate intralocus sexual conflict in seed beetles

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.     

PERCHED AT THE MITO‐NUCLEAR CROSSROADS: DIVERGENT MITOCHONDRIAL LINEAGES CORRELATE WITH ENVIRONMENT IN THE FACE OF ONGOING NUCLEAR GENE FLOW IN AN AUSTRALIAN BIRD

Relationships among multilocus genetic variation, geography, and environment can reveal how evolutionary processes affect genomes. We examined the evolution of an Australian bird, the eastern yellow robin Eopsaltria australis, using mitochondrial (mtDNA) and nuclear (nDNA) genetic markers, and bioclimatic variables. In southeastern Australia, two divergent mtDNA lineages occur east and west of the Great Dividing Range, perpendicular to latitudinal nDNA structure. We evaluated alternative scenarios to explain this striking discordance in landscape genetic patterning. Stochastic mtDNA lineage sorting can be rejected because the mtDNA lineages are essentially distinct geographically for > 1500 km. Vicariance is unlikely: the Great Dividing Range is neither a current barrier nor was it at the Last Glacial Maximum according to species distribution modeling; nuclear gene flow inferred from coalescent analysis affirms this. Female philopatry contradicts known female‐biased dispersal. Contrasting mtDNA and nDNA demographies indicate their evolutionary histories are decoupled. Distance‐based redundancy analysis, in which environmental temperatures explain mtDNA variance above that explained by geographic position and isolation‐by‐distance, favors a nonneutral explanation for mitochondrial phylogeographic patterning. Thus, observed mito‐nuclear discordance accords with environmental selection on a female‐linked trait, such as mtDNA, mtDNA–nDNA interactions or genes on W‐chromosome, driving mitochondrial divergence in the presence of nuclear gene flow.     

Pervasive adaptive evolution in primate seminal proteins

Seminal fluid proteins show striking effects on reproduction, involving manipulation of female behavior and physiology, mechanisms of sperm competition, and pathogen defense. Strong adaptive pressures are expected for such manifestations of sexual selection and host defense, but the extent of positive selection in seminal fluid proteins from divergent taxa is unknown. We identified adaptive evolution in primate seminal proteins using genomic resources in a tissue-specific study. We found extensive signatures of positive selection when comparing 161 human seminal fluid proteins and 2,858 prostate-expressed genes to those in chimpanzee. Seven of eight outstanding genes yielded statistically significant evidence of positive selection when analyzed in divergent primates. Functional clues were gained through divergent analysis, including several cases of species-specific loss of function in copulatory plug genes, and statistically significant spatial clustering of positively selected sites near the active site of kallikrein 2. This study reveals previously unidentified positive selection in seven primate seminal proteins, and when considered with findings in Drosophila, indicates that extensive positive selection is found in seminal fluid across divergent taxonomic groups.     

Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations

Many conserved eukaryotic traits, including apoptosis, two sexes, speciation and ageing, can be causally linked to a bioenergetic requirement for mitochondrial genes. Mitochondrial genes encode proteins involved in cell respiration, which interact closely with proteins encoded by nuclear genes. Functional respiration requires the coadaptation of mitochondrial and nuclear genes, despite divergent tempi and modes of evolution. Free-radical signals emerge directly from the biophysics of mosaic respiratory chains encoded by two genomes prone to mismatch, with apoptosis being the default penalty for compromised respiration. Selection for genomic matching is facilitated by two sexes, and optimizes fitness, adaptability and fertility in youth. Mismatches cause infertility, low fitness, hybrid breakdown, and potentially speciation. The dynamics of selection for mitonuclear function optimize fitness over generations, but the same selective processes also operate within generations, driving ageing and age-related diseases. This coherent view of eukaryotic energetics offers striking insights into infertility and age-related diseases.     

Comparative genomics and the evolution of human mitochondrial DNA: assessing the effects of selection

This article provides evidence that selection has been a significant force during the evolution of the human mitochondrial genome. Both gene-by-gene and whole-genome approaches were used here to assess selection in the 560 mitochondrial DNA (mtDNA) coding-region sequences that were used previously for reduced-median-network analysis. The results of the present analyses were complex, in that the action of selection was not indicated by all tests, but this is not surprising, in view of the characteristics and limitations of the different analytical methods. Despite these limitations, there is evidence for both gene-specific and lineage-specific variation in selection. Whole-genome sliding-window approaches indicated a lack of selection in large-scale segments of the coding region. In other tests, we analyzed the ratio of nonsynonymous-to-synonymous substitutions in the 13 protein-encoding mtDNA genes. The most straightforward interpretation of those results is that negative selection has acted on the mtDNA during evolution. Single-gene analyses indicated significant departures from neutrality in the CO1, ND4, and ND6 genes, although the data also suggested the possible operation of positive selection on the AT6 gene. Finally, our results and those of other investigators do not support a simple model in which climatic adaptation has been a major force during human mtDNA evolution.     

Steep,coincident, and concordant clines in mitochondrial and nuclear‐encoded genes in a hybrid zone between subspecies of Atlantic killifish,Fundulus heteroclitus

Steep genetic clines resulting from recent secondary contact between previously isolated taxa can either gradually erode over time or be stabilized by factors such as ecological selection or selection against hybrids. We used patterns of variation in 30 nuclear and two mitochondrial SNPs to examine the factors that could be involved in stabilizing clines across a hybrid zone between two subspecies of the Atlantic killifish, Fundulus heteroclitus. Increased heterozygote deficit and cytonuclear disequilibrium in populations near the center of the mtDNA cline suggest that some form of reproductive isolation such as assortative mating or selection against hybrids may be acting in this hybrid zone. However, only a small number of loci exhibited these signatures, suggesting locus‐specific, rather than genomewide, factors. Fourteen of the 32 loci surveyed had cline widths inconsistent with neutral expectations, with two SNPs in the mitochondrial genome exhibiting the steepest clines. Seven of the 12 putatively non‐neutral nuclear clines were for SNPs in genes related to oxidative metabolism. Among these putatively non‐neutral nuclear clines, SNPs in two nuclear‐encoded mitochondrial genes (SLC25A3 and HDDC2), as well as SNPs in the myoglobin, 40S ribosomal protein S17, and actin‐binding LIM protein genes, had clines that were coincident and concordant with the mitochondrial clines. When hybrid index was calculated using this subset of loci, the frequency distribution of hybrid indices for a population located at the mtDNA cline center was non‐unimodal, suggesting selection against advanced‐generation hybrids, possibly due to effects on processes involved in oxidative metabolism.