Urban Friberg

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to traditional explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side–effect of females evolving to reduce the direct costs of mating.

Evolutionary implications of non-neutral mitochondrial genetic variation

Sequence variation in mitochondrial DNA (mtDNA) was traditionally considered to be selectively neutral. However, an accumulating body of evidence indicates that this assumption is invalid. Furthermore, recent advances indicate that mtDNA polymorphism can be maintained within populations via selection on the joint mitochondrial-nuclear genotype. Here, we review the latest findings that show mitochondrial and cytoplasmic genetic variation for life-history traits and fitness. We highlight the key importance of the mitochondrial-nuclear interaction as a unit of selection and discuss the consequences of mitochondrially encoded fitness effects on several key evolutionary processes. Our goal is to draw attention to the profound, yet neglected, influence of the mitochondrial genome on the fields of ecology and evolution.

Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females

The evolution of female mate choice, broadly defined to include any female behaviour or morphology which biases matings towards certain male phenotypes, is traditionally thought to result from direct or indirect benefits which females acquire when mating with preferred males. In contrast, new models have shown that female mate choice can be generated by sexual conflict, where preferred males may cause a fitness depression in females. Several studies have shown that female Drosophila melanogaster bias matings towards large males. Here, we use male size as a proxy for male attractiveness and test how female fitness is affected by reproducing with large or small males, under two different male densities. Females housed with large males had reduced lifespan and aged at an accelerated rate compared with females housed with small males, and increased male density depressed female fitness further. These fitness differences were due to effects on several different fitness components. Female fitness covaried negatively with male courtship rate, which suggests a cost of courtship. Mating rate increased with male size, whereas female fitness peaked at an intermediate mating rate. Our results suggest that female mate choice in D. melanogaster is, at least in part, a by‐product of sexual conflict over the mating rate.

Male perception of female mating status: its effect on copulation duration, sperm defence and female fitness

When females mate with multiple partners, the risk of sperm competition depends on female mating history. To maximize fitness, males should adjust their copulatory investments according to this risk. In the fruit fly, Drosophila melanogaster, the female cuticular hydrocarbon (CH) profile changes when females mate, and males use this to assess female mating status. I tested whether this cue influenced the time males spent copulating with females and if this affected male fertilization success and female fitness. I manipulated female mating status by transferring CHs from either virgin or mated females to virgin females. Males copulated significantly longer with virgin females that had been coated with CHs from mated females (experimental group) than with virgin females coated with CHs from other virgin females (control group). Copulation duration did not differ between females from the experimental group and females that had already mated. To test whether differential investment in copulation affected male sperm defence and female fitness, experimental and control females were mated once to wild-type males and then either housed with males carrying a genetic marker (experiment 1) or alone (experiment 2). In experiment 1 male sperm defence was elevated when males perceived their partner as mated, and this was mainly due to females remating less. Increased male investment in copulation duration also affected female fitness, although this was reversed between experiments 1 and 2. Finally, these results also indicate that copulations are costly to males, since manipulated males copulated for longer with virgin females than they normally would, resulting in higher fertilization success.

Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster.

The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.

Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation

Abstract In promiscuous species, sexual selection generates two opposing male traits: offense (acquiring new mates and supplanting stored sperm) and defense (enforcing fidelity on ones mates and preventing sperm displacement when this fails). Coevolution between these traits requires both additive genetic variation and associated natural selection. Previous work with Drosophila melanogaster found autosomal genetic variation for these traits among inbred lines from a mixture of populations, but only nonheritable genetic variation was found within a single outbred population. These results do not support ongoing antagonistic coevolution between offense and defense, nor between either of these male traits and female reproductive characters. Here we use a new method (hemiclonal analysis) to study genomewide genetic variation in a large outbred laboratory population of D. melanogaster. Hemiclonal analysis estimates the additive genetic variation among random, genomewide haplotypes taken from a large, outbred, locally adapted laboratory population and determines the direction of the selection gradient on this variation. In contrast to earlier studies, we found low but biologically significant heritable variation for defensive and offensive offspring production as well as all their components (P1, fidelity, P2, and remating). Genetic correlations between these traits were substantially different from those reported for inbred lines. A positive genetic correlation was found between defense and offense, demonstrating that some shared genes influence both traits. In addition to this common variation, evidence for unique genetic variation for each trait was also found, supporting an ongoing coevolutionary arms race between defense and offense. Reproductive conflict between males can strongly influence female fitness. Correspondingly, we found genetic variation in both defense and offense that affected female fitness. No evidence was found for intersexual conflict in the context of male defense, but we found substantial intersexual conflict in the context of male offensive sperm competitive ability. These results indicate that conflict between competing males also promotes an associated arms race between the sexes.

Sex differences in the genetic architecture of lifespan in a seed beetle : extreme inbreeding extends male lifespan

BackgroundSex 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.ResultsHere 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.ConclusionNo 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.

HOMOSEXUALITY AS A CONSEQUENCE OF EPIGENETICALLY CANALIZED SEXUAL DEVELOPMENT

Male and female homosexuality have substantial prevalence in humans. Pedigree and twin studies indicate that homosexuality has substantial heritability in both sexes, yet concordance between identical twins is low and molecular studies have failed to find associated DNA markers. This paradoxical pattern calls for an explanation. We use published data on fetal androgen signaling and gene regulation via nongenetic changes in DNA packaging (epigenetics) to develop a new model for homosexuality. It is well established that fetal androgen signaling strongly influences sexual development. We show that an unappreciated feature of this process is reduced androgen sensitivity in XX fetuses and enhanced sensitivity in XY fetuses, and that this difference is most feasibly caused by numerous sex-specific epigenetic modifications (“epi-marks”) originating in embryonic stem cells. These epi-marks buffer XX fetuses from masculinization due to excess fetal androgen exposure and similarly buffer XY fetuses from androgen underexposure. Extant data indicates that individual epi-marks influence some but not other sexually dimorphic traits, vary in strength across individuals, and are produced during ontogeny and erased between generations. Those that escape erasure will steer development of the sexual phenotypes they influence in a gonad-discordant direction in opposite sex offspring, mosaically feminizing XY offspring and masculinizing XX offspring. Such sex-specific epi-marks are sexually antagonistic (SA-epi-marks) because they canalize sexual development in the parent that produced them, but contribute to gonad-trait discordances in opposite-sex offspring when unerased. In this model, homosexuality occurs when stronger-than-average SA-epi-marks (influencing sexual preference) from an opposite-sex parent escape erasure and are then paired with a weaker-than-average de novo sex-specific epi-marks produced in opposite-sex offspring. Our model predicts that homosexuality is part of a wider phenomenon in which recently evolved androgen-influenced traits commonly display gonad-trait discordances at substantial frequency, and that the molecular feature underlying most homosexuality is not DNA polymorphism(s), but epi-marks that evolved to canalize sexual dimorphic development that sometimes carryover across generations and contribute to gonad-trait discordances in opposite-sex descendants.

The Shared Genome Is a Pervasive Constraint on the Evolution of Sex-Biased Gene Expression

Males and females share most of their genomes, and differences between the sexes can therefore not evolve through sequence divergence in protein coding genes. Sexual dimorphism is instead restricted to occur through sex-specific expression and splicing of gene products. Evolution of sexual dimorphism through these mechanisms should, however, also be constrained when the sexes share the genetic architecture for regulation of gene expression. Despite these obstacles, sexual dimorphism is prevalent in the animal kingdom and commonly evolves rapidly. Here, we ask whether the genetic architecture of gene expression is plastic and easily molded by sex-specific selection, or if sexual dimorphism evolves rapidly despite pervasive genetic constraint. To address this question, we explore the relationship between the intersexual genetic correlation for gene expression (rMF), which captures how independently genes are regulated in the sexes, and the evolution of sex-biased gene expression. Using transcriptome data from Drosophila melanogaster, we find that most genes have a high rMF and that genes currently exposed to sexually antagonistic selection have a higher average rMF than other genes. We further show that genes with a high rMF have less pronounced sex-biased gene expression than genes with a low rMF within D. melanogaster and that the strength of the rMF in D. melanogaster predicts the degree to which the sex bias of a genes expression has changed between D. melanogaster and six other species in the Drosophila genus. In sum, our results show that a shared genome constrains both short- and long-term evolution of sexual dimorphism.

The genetic architecture of fitness in a seed beetle: assessing the potential for indirect genetic benefits of female choice

BackgroundQuantifying the amount of standing genetic variation in fitness represents an empirical challenge. Unfortunately, the shortage of detailed studies of the genetic architecture of fitness has hampered progress in several domains of evolutionary biology. One such area is the study of sexual selection. In particular, the evolution of adaptive female choice by indirect genetic benefits relies on the presence of genetic variation for fitness. Female choice by genetic benefits fall broadly into good genes (additive) models and compatibility (non-additive) models where the strength of selection is dictated by the genetic architecture of fitness. To characterize the genetic architecture of fitness, we employed a quantitative genetic design (the diallel cross) in a population of the seed beetle Callosobruchus maculatus, which is known to exhibit post-copulatory female choice. From reciprocal crosses of inbred lines, we assayed egg production, egg-to-adult survival, and lifetime offspring production of the outbred F1 daughters (F1 productivity).ResultsWe used the bio model to estimate six components of genetic and environmental variance in fitness. We found sizeable additive and non-additive genetic variance in F1 productivity, but lower genetic variance in egg-to-adult survival, which was strongly influenced by maternal and paternal effects.ConclusionOur results show that, in order to gain a relevant understanding of the genetic architecture of fitness, measures of offspring fitness should be inclusive and should include quantifications of offspring reproductive success. We note that our estimate of additive genetic variance in F1 productivity (CVA= 14%) is sufficient to generate indirect selection on female choice. However, our results also show that the major determinant of offspring fitness is the genetic interaction between parental genomes, as indicated by large amounts of non-additive genetic variance (dominance and/or epistasis) for F1 productivity. We discuss the processes that may maintain additive and non-additive genetic variance for fitness and how these relate to indirect selection for female choice.