Male Fitness Components Research Articles

Sexually concordant selection on floral traits despite greater opportunity for selection through male fitness.

Pollinators are important drivers of floral trait evolution, yet plant populations are not always perfectly adapted to their pollinators. Such apparent maladaptation may result from conflicting selection through male and female sexual functions in hermaphrodites. We studied sex-specific mating patterns and phenotypic selection on floral traits in Aconitum gymnandrum. After genotyping 1786 offspring, we partitioned individual fitness into sex-specific selfed and outcrossed components and estimated phenotypic selection acting through each. Relative fitness increased with increasing mate number, and more so for male function. This led to greater opportunity for selection through outcrossed male fitness, though patterns of phenotypic selection on floral traits tended to be similar, and with better support for selection through female rather than male fitness components. We detected directional selection through one or more fitness component for larger flower number, larger flowers, and more negative nectar gradients within inflorescences. Our results are consistent with Bateman's principles for sex-specific mating patterns and illustrate that, despite the expected difference in opportunity for selection, patterns of variation in selection across traits can be rather similar for the male and female sexual functions. These results shed new light on the effect of sexual selection on the evolution of floral traits.

Mating traits are phenotypically but not genetically correlated to fitness

AbstractMisalignment between male and female interests over mating creates interlocus sexual conflict that is known to drive the coevolution of reproductive traits. Males and females also share the majority of their genome, which may cause these traits to be genetically covary between the sexes and experience intralocus sexual conflict where beneficial alleles in one sex are costly when expressed in the other. Here, we use a quantitative genetic experiment to test whether intralocus sexual conflict is operating on mating latency and copulation duration in the polyandrous fruit-fly Drosophila serrata. We performed two paternal half-sibling breeding designs in different populations and measured mating latency and copulation duration in males and females, and components of pre- and postcopulatory fitness in both sexes. Our design enabled the estimation of selection on mating latency and copulation duration and the heritabilities, and within-sex and across-sex genetic covariances of these traits. Mating latency and copulation duration were both heritable in males but not in females, and within sex and across-sex genetic correlations among the traits were all small. Despite significant phenotypic correlations between these mating traits and some male and female fitness components, we found no significant genetic covariance between any measured mating behaviors and fitness components, nor between male and female fitness. Our study, therefore, finds little evidence of ongoing intralocus sexual conflict over these traits. One explanation for our result is that these mating traits have been under strong selection, which has exhausted their genetic variation, limiting their ability to respond to ongoing selection.

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite.

Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separate-sexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

A decade of sexual selection studies reveals patterns and processes of fitness variation in male collared lizards

Territory defence is widely assumed to be adaptive because it enhances reproductive success. However, empirical evidence for such a benefit is scarce or nonexistent for many types of territorial organisms. The roles of intraspecific aggression versus interactions with females in successful breeding by territorial males are also still poorly understood in lower tetrapods, including lizards. We address both of these important issues using 10 years of data on genetic parentage combined with field behavioural studies in collared lizards, Crotaphytus collaris . As predicted, territorial males (T-males) had more mates, sired markedly more total offspring and sired more surviving offspring with more females than did nonterritorial (NT) males. Territorial males in structurally simpler habitats sired a higher proportion of each female's offspring than their counterparts in complex habitats, indicating that the ability of T-males to accrue mating benefits is highest where topography maximizes contact with multiple females. All measures of T-male reproductive success increased with travel rate but decreased with the time spent courting individual females, suggesting a fitness trade-off between these behaviours. We found no evidence that aggressive behaviour was linked to any component of male fitness. Hence, activities of territory owners appear to be shaped by sexual selection to enhance mating opportunities rather than to aggressively dominate same-sex rivals. Our study illustrates the value of long-term research documenting behaviour and fitness of free-ranging individuals over multiple reproductive cycles in evaluating fundamental questions about the adaptive significance of social tactics. • Territorial male collared lizards had higher fitness than nonterritorial males. • Territorial tactics increased mating more effectively in simpler habitats. • Fitness of territory owners increased with travel but not with aggressive behaviour. • Limiting courtship per female promoted travel to interact with additional mates. • Male behaviour is selected to enhance interactions with multiple female mates.

Quantifying the costs of pre- and postcopulatory traits for males: Evidence that costs of ejaculation are minor relative to mating effort.

Although it is widely stated that both mating behavior and sperm traits are energetically costly for males, we currently lack empirical estimates of the relative costs to males of pre‐ versus postcopulatory investments. Such estimates require the experimental separation of the act of mating from that of ejaculation, which is a nontrivial logistical challenge. Here, we overcome this challenge using a novel morphological manipulation (gonopodium tip ablation) in the eastern mosquitofish (Gambusia holbrooki) to tease apart investment in mating effort from that in sperm replenishment following ejaculation. We quantified the relative cumulative costs of investing in mating effort and ejaculation by comparing somatic traits and reproductive performance among three types of males: ablated males that could attempt to mate but not ejaculate; unablated males that could both mate and ejaculate; and control males that had no access to females. We show that, after eight weeks, mating investment significantly reduces both body growth and immunocompetence and results in a significant decline in mating effort. In contrast, cumulative investment into sperm replenishment following ejaculation has few detectable effects that are only apparent in smaller males. These minor costs occur despite the fact that G. holbrooki has very high levels of sperm competition and multiple mating by both sexes, which is usually associated with elevated levels of sperm production. Crucially, our study is the first, to our knowledge, to experimentally compare the relative costs of pre‐ and postcopulatory investment on components of male fitness in a vertebrate.

The repeatable opportunity for selection differs between pre- and postcopulatory fitness components.

In species with multiple mating, intense sexual selection may occur both before and after copulation. However, comparing the strength of pre‐ and postcopulatory selection is challenging, because (i) postcopulatory processes are generally difficult to observe and (ii) the often‐used opportunity for selection (I) metric contains both deterministic and stochastic components. Here, we quantified pre‐ and postcopulatory male fitness components of the simultaneously hermaphroditic flatworm, Macrostomum lignano. We did this by tracking fluorescent sperm—using transgenics—through the transparent body of sperm recipients, enabling to observe postcopulatory processes in vivo. Moreover, we sequentially exposed focal worms to three independent mating groups, and in each assessed their mating success, sperm‐transfer efficiency, sperm fertilizing efficiency, and partner fecundity. Based on these multiple measures, we could, for each fitness component, combine the variance (I) with the repeatability (R) in individual success to assess the amount of repeatable variance in individual success—a measure we call the repeatable opportunity for selection (IR). We found higher repeatable opportunity for selection in sperm‐transfer efficiency and sperm fertilizing efficiency compared to mating success, which clearly suggests that postcopulatory selection is stronger than precopulatory selection. Our study demonstrates that the opportunity for selection contains a repeatable deterministic component, which can be assessed and disentangled from the often large stochastic component, to provide a better estimate of the strength of selection.

Bee-Mediated Selection Favors Floral Sex Specialization in a Heterantherous Species: Strategies to Solve the Pollen Dilemma.

Animal-pollinated plants show a broad variation in floral morphology traits and gametophyte production within populations. Thus, floral traits related to plant reproduction and sexuality are usually exposed to pollinator-mediated selection. Such selective pressures may be even stronger in heterantherous and pollen flowers, in which pollen contributes to both bee feeding and pollination, overcoming the “pollen dilemma” or the inability to perform both functions simultaneously. We describe the phenotypic gender and sexual organ morphology of flowers in two populations of Macairea radula (Melastomataceae), a heterantherous and buzz-pollinated species with pollen flowers. We estimated selection gradients on these traits through female and male fitness components. Both populations showed sizeable phenotypic gender variation, from strict hermaphrodites to increased femaleness or maleness. We found a continuous variation in style and stamen size, and this variation was correlated with corresponding shape values of both sexual organs. We detected bee-mediated selection towards short and long styles through seed number and towards intermediate degrees of heteranthery through pollen removal in one population, and selection towards increased maleness through pollen dispersal in both populations. Our results suggest that bee-mediated selection favors floral sex specialization and stylar dimorphism in M. radula, optimizing reproductive success and solving the pollen dilemma.

Effects of herbivory and its timing on reproductive success of a tropical deciduous tree.

The implications of herbivory for plant reproduction have been widely studied; however, the relationship of defoliation and reproductive success is not linear, as there are many interacting factors that may influence reproductive responses to herbivore damage. In this study we aimed to disentangle how the timing of foliar damage impacts both male and female components of fitness, and to assess when it has greater impacts on plant reproductive success. We measured herbivore damage and its effects on floral production, male and female floral attributes as well as fruit yield in three different phenological phases of Casearia nitida (Salicaceae) over the course of two consecutive years. Then we tested two models of multiple causal links among herbivory and reproductive success using piecewise structural equation models. The effects of leaf damage differed between reproductive seasons and between male and female components of fitness. Moreover, the impact of herbivory extended beyond the year when it was exerted. The previous season's cumulated foliar damage had the largest impact on reproductive characters, in particular a negative effect on the numbers of inflorescences, flowers and pollen grains, indirectly affecting the numbers of infructescences and fruits, and a positive one on the amount of foliar damage during flowering. For perennial and proleptic species, the dynamics of resource acquisition and allocation patterns for reproduction promote and extend the effects of herbivore damage to longer periods than a single reproductive event and growing season, through the interactions among different components of female and male fitness.

Condition-dependent mortality exacerbates male (but not female) reproductive senescence and the potential for sexual conflict.

Disentangling the relationship between age and reproduction is central to understand life-history evolution, and recent evidence shows that considering condition-dependent mortality is a crucial piece of this puzzle. For example, nonrandom mortality of 'low-condition' individuals can lead to an increase in average lifespan. However, selective disappearance of such low-condition individuals may also affect reproductive senescence at the population level due to trade-offs between physiological functions related to survival/lifespan and the maintenance of reproductive functions. Here, we address the idea that condition-dependent extrinsic mortality (i.e. simulated predation) may increase the age-related decline in male reproductive success and with it the potential for sexual conflict, by comparing reproductive ageing in Drosophila melanogaster male/female cohorts exposed (or not) to condition-dependent simulated predation across time. Although female reproductive senescence was not affected by predation, male reproductive senescence was considerably higher under predation, due mainly to an accelerated decline in offspring viability of 'surviving' males with age. This sex-specific effect suggests that condition-dependent extrinsic mortality can exacerbate survival-reproduction trade-offs in males, which are typically under stronger condition-dependent selection than females. Interestingly, condition-dependent extrinsic mortality did not affect mating success, hinting that accelerated reproductive senescence is due to a decrease in male post-copulatory fitness components. Our results support the recent proposal that male ageing can be an important source of sexual conflict, further suggesting this effect could be exacerbated under more natural conditions.

Differential investment in pre- and post-mating male sexual traits in response to prolonged exposure to ambient UVB radiation in a fish

Increasing UVB radiation (UVB) reaching earth's surface following stratospheric ozone depletion is linked to serious consequences for organisms. While studies have focused on direct cytocidal and immunomodulatory effects of UVB, indirect consequences for fitness-related life-history traits are largely unexplored, although knowledge is needed to understand organismal responses to climate change. The present study investigates the effects of developmental exposure to enhanced, but ecologically relevant, ambient UVB levels on growth (body size), parental behavior (nest-building), fitness-enhancing traits of pre-mating (sexual ornamentation) and post-mating (sperm traits) sexual selection as well as their interrelationships in male three-spined sticklebacks (Gasterosteus aculeatus). Moreover, potentially underlying direct UVB effects, testicular antioxidant capacity (TAC) and testes and skin melanization were quantified. Juvenile full-siblings were split into two groups and raised until adulthood in a semi-natural set-up under light conditions including either natural (UVBnormal) or elevated UVB levels (UVBenhanced). When becoming reproductive, males were kept individually before data collection took place at their reproductive peak. The results showed that males from the UVBenhanced-group were smaller than their brothers from the UVBnormal-treatment, whereas no treatment differences were observed for sexual ornamentation, sperm traits and TAC. Moreover, UVB-stressed males built their nests faster and the relationship between body size and nest size was negative for UVBenhanced-males while being positive for UVBnormal-males. These results demonstrate that, depending on physical state, UVB-stressed males adjusted their behavior to some extent. Additionally, a trade-off between the investment in pre- and post-mating traits was found for UVBenhanced-males, i.e. the intensity of their breeding coloration was negatively correlated with sperm number whereas this relationship was reversed for UVBnormal-males, thus showing an interaction between pre- and post-mating traits regarding exposure treatment. The interaction provides first experimental evidence that differential allocation to energetically demanding pre- and post-mating components of male fitness is triggered by a key environmental stressor of climate change.

Complex interactions between sperm viability and female fertility

Sperm viability is a major male fitness component, with higher sperm viability associated with enhanced sperm competitiveness. While many studies have focussed on sperm viability from the male fitness standpoint, its impact on female fitness is less clear. Here we used a panel of 32 isogenic Drosophila simulans lines to test for genetic variation in sperm viability (percentage of viable cells). We then tested whether sperm viability affected female fitness by mating females to males from low or high sperm viability genotypes. We found significant variation in sperm viability among genotypes, and consistent with this, sperm viability was highly repeatable within genotypes. Additionally, females mated to high sperm viability males laid more eggs in the first seven hours after mating, and produced more offspring in total. However, the early increase in oviposition did not result in more offspring in the 8 hours following mating, suggesting that mating with high sperm-viability genotypes leads to egg wastage for females shortly after copulation. Although mating with high sperm-viability males resulted in higher female fitness in the long term, high quality ejaculates would result in a short-term female fitness penalty, or at least lower realised fitness, potentially generating sexual conflict over optimal sperm viability.

Sex differences in local adaptation: what can we learn from reciprocal transplant experiments?

Local adaptation is of fundamental interest to evolutionary biologists. Traditionally, local adaptation has been studied using reciprocal transplant experiments to quantify fitness differences between residents and immigrants in pairwise transplants between study populations. Previous studies have detected local adaptation in some cases, but others have shown lack of adaptation or even maladaptation. Recently, the importance of different fitness components, such as survival and fecundity, to local adaptation have been emphasized. Here, we address another neglected aspect in studies of local adaptation: sex differences. Given the ubiquity of sexual dimorphism in life histories and phenotypic traits, this neglect is surprising, but may be partly explained by differences in research traditions and terminology in the fields of local adaptation and sexual selection. Studies that investigate differences in mating success between resident and immigrants across populations tend to be framed in terms of reproductive and behavioural isolation, rather than local adaptation. We briefly review the published literature that bridges these areas and suggest that reciprocal transplant experiments could benefit from quantifying both male and female fitness components. Such a more integrative research approach could clarify the role of sex differences in the evolution of local adaptations.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

The interaction between sex-specific selection and local adaptation in species without separate sexes.

Local adaptation in hermaphrodite species can be based on a variety of fitness components, including survival, as well as both female and male sex-functions within individuals. When selection via female and male fitness components varies spatially (e.g. due to environmental heterogeneity), local adaptation will depend, in part, on variation in selection through each fitness component, and the extent to which genetic trade-offs between sex-functions maintain genetic variation necessary for adaptation. Local adaptation will also depend on the hermaphrodite mating system because self-fertilization alters several key factors influencing selection and the maintenance of genetic variance underlying trade-offs between the sex-functions (sexually antagonistic polymorphism). As a first step to guide intuition regarding sex-specific adaptation in hermaphrodites, we develop a simple theoretical model incorporating the essential features of hermaphrodite mating and adaptation in a spatially heterogeneous environment, and explore the interaction between sex-specific selection, self-fertilization and local adaptation. Our results suggest that opportunities for sex-specific local adaptation in hermaphrodites depend strongly on the extent of self-fertilization and inbreeding depression. Using our model as a conceptual framework, we provide a broad overview of the literature on sex-specific selection and local adaptation in hermaphroditic plants and animals, emphasizing promising future directions in light of our theoretical predictions.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Death of new microRNA genes in Drosophila via gradual loss of fitness advantages.

The prevalence of de novo coding genes is controversial due to length and coding constraints. Noncoding genes, especially small ones, are freer to evolve de novo by comparison. The best examples are microRNAs (miRNAs), a large class of regulatory molecules ∼22 nt in length. Here, we study six de novo miRNAs in Drosophila, which, like most new genes, are testis-specific. We ask how and why de novo genes die because gene death must be sufficiently frequent to balance the many new births. By knocking out each miRNA gene, we analyzed their contributions to the nine components of male fitness (sperm production, length, and competitiveness, among others). To our surprise, the knockout mutants often perform better than the wild type in some components, and slightly worse in others. When two of the younger miRNAs are assayed in long-term laboratory populations, their total fitness contributions are found to be essentially zero. These results collectively suggest that adaptive de novo genes die regularly, not due to the loss of functionality, but due to the canceling out of positive and negative fitness effects, which may be characterized as “quasi-neutrality.” Since de novo genes often emerge adaptively and become lost later, they reveal ongoing period-specific adaptations, reminiscent of the “Red-Queen” metaphor for long-term evolution.

Consequences of secondary nectar robbing for male components of plant reproduction.

Organisms engage in multiple species interactions simultaneously. While pollination studies generally focus on plants and pollinators exclusively, secondary robbing, a behavior that requires other species (primary robbers) to first create access holes in corollas, is common. It has been shown that secondary robbing can reduce plants' female fitness; however, we lack knowledge about its impact on male plant fitness. We experimentally simulated primary and secondary robbing in the monocarpic perennial Ipomopsis aggregata (Polemoniaceae), quantifying indirect effects on pollinator-mediated pollen (dye) donation. We also assessed whether continual nectar removal via the floral opening has similar effects on hummingbird-pollinator behavior as continual secondary robbing through robber holes. We found no significant indirect effects of secondary robbing on a component of Ipomopsis male fitness. Although robbing did reduce pollen (dye) donation due to avoidance of robbed plants by pollinating hummingbirds, pollen donation did not differ between the two robbing treatments. The effects of secondary robbing on hummingbird behavior resembled effects of chronic nectar removal by pollinators. Our results indicate that hummingbird pollinators may use a combination of cues, including cues given by the presence or absence of nectar, to make foraging decisions. Combined with prior research, this study suggests that secondary robbing is less costly to a component of male fitness than to female fitness in Ipomopsis, broadening our knowledge of the overall costs of mutualism exploitation to total plant fitness.

Coadaptation of mitochondrial and nuclear genes, and the cost of mother's curse.

Strict maternal inheritance renders the mitochondrial genome susceptible to accumulating mutations that harm males, but are otherwise benign or beneficial for females. This 'mother's curse' effect can degrade male survival and fertility if unopposed by counteracting evolutionary processes. Coadaptation between nuclear and mitochondrial genomes-with nuclear genes evolving to compensate for male-harming mitochondrial substitutions-may ultimately resolve mother's curse. However, males are still expected to incur a transient fitness cost during mito-nuclear coevolution, and it remains unclear how severe such costs should be. We present a population genetic analysis of mito-nuclear coadaptation to resolve mother's curse effects, and show that the magnitude of the 'male mitochondrial load'-the negative impact of mitochondrial substitutions on male fitness components-may be large, even when genetic variation for compensatory evolution is abundant. We also find that the male load is surprisingly sensitive to population size: male fitness costs of mito-nuclear coevolution are particularly pronounced in both small and large populations, and minimized in populations of intermediate size. Our results reveal complex interactions between demography and genetic constraints during the resolution of mother's curse, suggesting potentially widespread species differences in susceptibility to mother's curse effects.

Body size evolution in an old insect order: No evidence for Cope's Rule in spite of fitness benefits of large size.

We integrate field data and phylogenetic comparative analyses to investigate causes of body size evolution and stasis in an old insect order: odonates ("dragonflies and damselflies"). Fossil evidence for "Cope's Rule" in odonates is weak or nonexistent since the last major extinction event 65 million years ago, yet selection studies show consistent positive selection for increased body size among adults. In particular, we find that large males in natural populations of the banded demoiselle (Calopteryx splendens) over several generations have consistent fitness benefits both in terms of survival and mating success. Additionally, there was no evidence for stabilizing or conflicting selection between fitness components within the adult life-stage. This lack of stabilizing selection during the adult life-stage was independently supported by a literature survey on different male and female fitness components from several odonate species. We did detect several significant body size shifts among extant taxa using comparative methods and a large new molecular phylogeny for odonates. We suggest that the lack of Cope's rule in odonates results from conflicting selection between fitness advantages of large adult size and costs of long larval development. We also discuss competing explanations for body size stasis in this insect group.

Experimental evidence for sexual selection against inbred males.

The detrimental effects of matings between relatives are well known. However, few studies determine the extent to which inbreeding depression in males is due to natural or sexual selection. Importantly, measuring fitness or key fitness components, rather than phenotypic traits allows more accurate estimation of inbreeding depression. We investigate how differences in inbreeding and juvenile diet (i.e. early stressful environment) influence a key component of male fitness, namely their reproductive success. We experimentally created inbred and outbred male mosquitofish (Gambusia holbrooki) by mating full-sibs (f=0·25). We show that this led to a 23% reduction in genome-wide heterozygosity based on SNPs. Males were raised on different diets early in life to create high-stress and low-stress rearing environments. We then allowed adult males to compete freely for females to test if inbreeding, early diet and their interaction affect a male's share of paternity. Early diet had no effect on paternity, but outbred males sired almost twice as many offspring as inbred males (n=628 offspring from 122 potential sires). Using artificial insemination methods we determined that this was unlikely to be due to early embryo mortality of eggs fertilised by inbred males: there was no evidence that male inbreeding status affects the realised fecundity of females (n=288). Given there was no difference in male mortality in our competitive mating experiment, the lower reproductive success of inbred males can most parsimoniously be attributed to inbreeding negatively affecting sexually selected traits that affect male mating success and/or sperm competitiveness. We discuss which sexually selected traits might be involved.

An Investigation of Tradeoffs in Herbicide Resistant <i>Brassica rapa</i>: Effects on Pollen and Ovule Production, Biomass and Development

For decades, herbicides have been used to control weeds and increase crop yields, a practice resulting in a growing number of weeds that are herbicide resistant. Like the problem of antibiotic resistance for medicine, herbicide resistant weeds present a significant agricultural challenge. To meet this challenge, we need management strategies informed by a more complete understanding of the biology of herbicide resistance. With this goal in mind we investigated tradeoffs in growth and reproduction of Atrazine Resistant (AR) versus Atrazine Susceptible (AS) Brassica rapa grown at two temperature regimes. Between the strains, tradeoffs were evident for pollen production and overall plant development. AS plants produced significantly more pollen per flower compared to AR plants. Additionally, development was significantly delayed in AR as compared to AS plants. Atrazine resistant plants took 20.5% longer than atrazine susceptible plants to produce their first true leaves, 13.0% longer to produce buds and 8% longer to produce the first flower as compared to the atrazine susceptible strain. Biomass, ovule count and pollen count were all greater in the cool treatment, however growth was significantly delayed as compared to the warm treatment. Plants in the cool treatment had significantly greater above ground biomass (26.5%) than plants in the warm treatment, but there was no effect of strain on biomass. Similarly, we found a significant effect of temperature, but not strain, on the average number of ovules produced per flower, with the warm treatment plants producing significantly fewer ovules than plants in the cool treatment. Warm temperatures also had a significant negative effect on pollen production. This study expands our understanding of tradeoffs associated with herbicide resistance to include effects on components of both male and female fitness.

A Segregating Inversion Generates Fitness Variation in Yellow Monkeyflower (Mimulus guttatus).

Polymorphic chromosomal rearrangements can bind hundreds of genes into single genetic loci with diverse effects. Rearrangements are often associated with local adaptation and speciation and may also be an important component of genetic variation within populations. We genetically and phenotypically characterize a segregating inversion (inv6) in the Iron Mountain (IM) population of Mimulus guttatus (yellow monkeyflower). We initially mapped inv6 as a region of recombination suppression in three F2 populations resulting from crosses among IM plants. In each case, the F1 parent was heterozygous for a derived haplotype, homogenous across markers spanning over 5 Mb of chromsome 6. In the three F2 populations, inv6 reduced male and female fitness components. In addition,i nv6 carriers suffered an ∼30% loss of pollen viability in the field. Despite these costs, inv6 exists at moderate frequency (∼8%) in the natural population, suggesting counterbalancing fitness benefits that maintain the polymorphism. Across 4 years of monitoring in the field, inv6 had an overall significant positive effect on seed production (lifetime female fitness) of carriers. This benefit was particularly strong in harsh years and may be mediated (in part) by strong positive effects on flower production. These data suggest that opposing fitness effects maintain an intermediate frequency, and as a consequence, inv6 generates inbreeding depression and high genetic variance. We discuss these findings in relation to the theory of inbreeding depression and the maintenance of fitness variation.