Genetic Benefits Research Articles

Consanguineous marriages: do genetic benefits outweigh its costs in populations with α +-thalassemia, hemoglobin S, and malaria?

Consanguinity is widespread in populations with endemic malaria. This practice, leading to an increase of homozygosis, could be either detrimental for lethal alleles (like hemoglobin S) or be potentially advantageous for beneficial alleles (like α +-thalassemia). The objective of this study was to analyze the effects of inbreeding on the fitness of a population with both, α +-thalassemia and hemoglobin S mutations. We calculated the relative fitness of an inbred population with α +-thalassemia and sickle cell anemia using a standard formula, and then compared it to that of an outbred population. An increase in the frequency of α +-thalassemia allele (0–1) results in a gain of relative fitness that is proportional to the coefficient of inbreeding; it is maximal at an allele frequency in the vicinity of 0.5. For hemoglobin S, an increase of frequency (0 to equilibrium point) produces a progressive loss of relative fitness that is also proportional to the coefficient of inbreeding; it is lowest at the equilibrium frequency that is always lower than 0.5. In a consanguineous population with both α +-thalassemia and hemoglobin S under selection pressure of malaria, the sum of contrary effects of inbreeding on the relative fitness of population depends on the frequencies of the two alleles and the coefficient of inbreeding.

Current analyses do not resolve whether extra-pair paternity is male or female driven

Recent studies question the importance of indirect genetic effects in explaining female benefits of extra-pair matings in socially monogamous species. Compiling data on 14 wild bird species, Arnqvist and Kirkpatrick (Am Nat 165:S26–S37, 2005) estimated the average direct cost in terms or reduced parental care to be an order of magnitude larger than the potential effect of genetic benefits. This study has sparked a debate regarding potential confounding factors but no consensus appears to have been reached. Here we focus on the implicit assumption that all individuals face the same selective pressures and argue that this assumption is probably too strong in most cases. Using a theoretical model we show that when the amount of resources that a male provides depends on territory quality, his physical condition or prospects for alternative breeding opportunities, a female may respond to such differences by altering her mating behaviour. Such confounding factors may lead to direct fitness effects that result in negative correlations between paternal care and paternity even if females that produce extra-pair young experience a net benefit. Negative correlations can also result when males forcefully seek copulations and females resist them. We discuss the studies included in the analysis in this light, and conclude that current analyses on the net selective pressures remain uninformative. In addition to considering average effects across individuals and species we suggest giving attention to individual differences and the influence of ecological factors such as territory quality and predation pressures on female mating behaviour.

Mate choice for non-additive genetic benefits: A resolution to the lek paradox

In promiscuous mating systems, females often show a consistent preference to mate with one or a few males, presumably to acquire heritable genetic benefits for their offspring. However, strong directional selection should deplete additive genetic variation in fitness and consequently any benefit to expressing the preference by females (referred to as the lek paradox). Here, we provide a novel resolution that examines non-additive genetic benefits, such as overdominance or inbreeding, as a source of genetic variation. Focusing on the inbreeding coefficient f and overdominance effects, we use dynamic models to show that (1) f can be inherited from sire to offspring, (2) populations with females that express a mating preferences for outbred males (low f) maintain higher genetic variation than populations with females that mate randomly, and (3) preference alleles for outbred males can invade populations even when the alleles are associated with a fecundity cost. We show that non-additive genetic variation due to overdominance can be converted to additive genetic variation and becomes “heritable” when the frequencies of alternative homozygous genotypes at fitness loci deviate from equality. Unlike previous models that assume an infinite population size, we now show that genetic drift in finite populations can lead to the necessary deviations in the frequencies of homozygous genotypes. We also show that the “heritability of f,” and hence the benefit to a mating preference for non-additive genetic benefits, is highest in small populations and populations in which a smaller number of loci contribute to fitness via overdominance. Our model contributes to the solution of the lek paradox.

Análise de níveis de significância genômica na identificação de marcadores moleculares em característica de baixa herdabilidade

Objetivou-se analisar diferentes níveis de significância na identificação de marcadores moleculares relacionados a uma característica quantitativa de baixa herdabilidade. Uma comparação entre os níveis de 1%, 5%, 10% e 20% foi realizada por meio do programa computacional de simulação genética (GENESYS), utilizando-se a seleção assistida por marcadores moleculares para avaliação desses níveis. Os resultados indicaram superioridade dos níveis de significância de maior magnitude (10% e 20%), em relação aos de menores valores (1% e 5%), quanto aos ganhos fenotípicos obtidos após a seleção, além de benefícios em alguns parâmetros genéticos (menor endogamia média; maior número de marcadores identificados e menor fixação de marcas). Assim, apesar de os níveis de 1% e 5% apresentarem uma maior precisão na detecção de marcadores – QTLs (quantitative trait loci), eles deixam a desejar no que diz respeito às melhorias genéticas, resultando em ganhos fenotípicos e genéticos inferiores.

Multiple paternity in reptiles: patterns and processes

The evolution of female promiscuity poses an intriguing problem as benefits of mating with multiple males often have to arise via indirect, genetic, effects. Studies on birds have documented that multiple paternity is common in natural populations but strong evidence for selection via female benefits is lacking. In an attempt to evaluate the evidence more broadly, we review studies of multiple paternity in natural populations of all major groups of nonavian reptiles. Multiple paternity has been documented in all species investigated so far and commonly exists in over 50% of clutches, with particularly high levels in snakes and lizards. Marine turtles and lizards with prolonged pair-bonding have relatively low levels of multiple paternity but levels are nevertheless higher than in many vertebrates with parental care. There is no evidence that high levels of polyandry are driven by direct benefits to females and the evidence that multiple paternity arises from indirect genetic benefits is weak. Instead, we argue that the most parsimonious explanation for patterns of multiple paternity is that it represents the combined effect of mate-encounter frequency and conflict over mating rates between males and females driven by large male benefits and relatively small female costs, with only weak selection via indirect benefits. A crucial step for researchers is to move from correlative approaches to experimental tests of assumptions and predictions of theory under natural settings, using a combination of molecular techniques and behavioural observations.

Female multiple mating and paternity in free-ranging North American red squirrels

Multimale mating (MMM) is common in female mammals, but our understanding of its evolutionary significance in this taxon lags behind that in others (e.g. invertebrates and birds). To date, the majority of research on mammalian MMM has been conducted under laboratory conditions, and the extent to which these findings have relevance for natural populations is little known. We quantified MMM in a free-ranging population of North American red squirrels, Tamiasciurus hudsonicus , and investigated its hypothesized influences and consequences. We observed 85 mating chases, representing 62 individual females, over three mating seasons and calculated standardized indexes of MMM and number of copulations. Extrinsic elements of mating chases (i.e. an index of the number of attending males and date) explained variation in MMM, while traits of the females (age and pre-oestrous body mass) did not correlate with MMM. Hypotheses of cryptic direct benefit (fertility assurance and infanticide avoidance) were not supported because MMM did not influence pregnancy rate, litter size or nest fate. There was also no correlation between MMM and offspring quality, multiple paternity or litter allelic diversity, and therefore, no support for hypotheses of genetic benefit. In addition to not accruing observable benefits to MMM, females did not incur a detectable cost, thus rendering MMM selectively neutral. Rather, in line with traditional explanations, female mating behaviour in red squirrels appears to be a passive response to selection on multifemale mating in males.

MHC-mediated mate choice increases parasite resistance in salmon

Natural (parasite-driven) and sexual selection are thought to maintain high polymorphism in the genes of the major histocompatibility complex (MHC), but support for a link between mate choice, MHC variation and increased parasite resistance is circumstantial. We compared MHC diversity and Anisakis loads among anadromous Atlantic salmon (Salmo salar L.) returning to four rivers to spawn, which had originated from natural spawning (parents allowed to mate freely) or artificial crosses (parents deprived from the potential benefits of mate choice). We found that the offspring of artificially bred salmon had higher parasite loads and were almost four times more likely to be infected than free-mating salmon, despite having similar levels of MHC diversity. Moreover, the offspring of wild salmon were more MHC dissimilar than the offspring of artificially crossed salmon, and uninfected fish were more dissimilar for MHC than infected fish. Thus, our results suggest a link between disassortative mating and offspring benefits and indicate that MHC-mediated mate choice and natural (parasite-driven) selection act in combination to maintain MHC diversity, and hence fitness. Therefore, artificial breeding programmes that negate the potential genetic benefits of mate choice may result in inherently inferior offspring, regardless of population size, rearing conditions or genetic diversity.

Female Promiscuity Does Not Lead to Increased Fertility or Fecundity in an Arctiid Moth (Utetheisa ornatrix)

Prior work has demonstrated significant phenotypic benefits to female promiscuity in the arctiid moth Utetheisa ornatrix. We were interested in determining whether U. ornatrix females also derive genetic benefits from mating multiply. We specifically tested whether, by mating with several males, females are able to exploit postcopulatory mechanisms that decrease the risk of fertilization by incompatible sperm. We show evidence that U. ornatrix females are not taking multiple mates as fertilization insurance because: (1) females that mate once are as fertile as those that mate three times; and (2) females that take three different mates are no more fertile than those that mate three times with the same male.

Local song elements indicate local genotypes and predict physiological condition in song sparrowsMelospiza melodia

Geographical variation in birdsong is taxonomically widespread and behaviourally salient, with females often preferring local over non-local song. However, the benefits associated with this preference remain poorly understood. One potential explanation is that song may reflect a male's place of origin and thus allow females to obtain genes well adapted to the local environment. We studied naturally occurring variation in the degree to which the elements of a male's song repertoire matched those of the local population ('syllable sharing') in migratory song sparrows (Melospiza melodia melodia). Syllable sharing was correlated with genetic similarity to the local population, suggesting that song reflects population of origin. Males sharing more syllables also had larger testosterone-dependent traits, fewer blood-borne parasites and reduced indicators of stress. Our findings are consistent with locally good genes models. Alternatively, immigrants' condition may suffer due to unfamiliarity with the breeding site or inability to match song elements during territorial interactions. Females preferring 'local-sounding' males may thus obtain genetic and/or direct benefits for their offspring.

Polyandry, sperm competition, and reproductive success in mice

Previous studies have attempted to assess the reproductive benefits of polyandry in mammals but have failed to account for variation in mating frequency across experimental treatments. Recently, it has been shown that multiply sired litters are common in natural populations of house mice, suggesting that female mice are actively polyandrous and sperm competition occurs in this species. Here we show that female house mice mated to 3 males (polyandry) had greater postbirth pup survival than females mated 3 times to the same male (monandry). Remote behavioral observations revealed that copulation frequency did not differ across our experimental treatments. We discuss this result with reference to genetic benefit hypotheses for the evolution of polyandry. Furthermore, by genotyping parents and offspring in the polyandrous treatment, we assessed which male reproductive traits contributed to paternity. We found that the first principal component describing variation in 10 male reproductive variables explained a significant proportion of the variation in paternity when males were second to mate. This component was weighted predominantly by measures of sperm length, suggesting that males with short sperm may be more successful when engaging in a disfavored role of sperm competition. Key words: genetic incompatibility, intrinsic sire effects, multiple mating, offspring viability, paternity, sperm size. [Behav Ecol]

Long-term fitness benefits of polyandry in a small mammal, the bank voleClethrionomys glareolus

Polyandry, i.e. mating with multiple males within one reproductive event, is a common female mating strategy but its adaptive function is often unclear. We tested whether polyandrous females gain genetic benefits by comparing fitness traits of monandrous (mated twice with a single male) and polyandrous (mated twice with two different males) female bank voles Clethrionomys glareolus. We raised the offspring in the laboratory until adulthood and measured their body size, before releasing them to outdoor enclosures to overwinter. At the onset of the breeding season in the following spring, we found that offspring of polyandrous females performed significantly better at reproduction than those of monandrous females. This was mainly due to sons of polyandrous females producing significantly more offspring than those of monandrous females. No significant differences were found for offspring body mass or winter survival between the two treatments. Our results appear to provide evidence that bank vole females gain long-term benefits from polyandry.

Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks

Multiple mating has clear fitness benefits for males, but uncertain benefits and costs for females. We tested for indirect genetic benefits of polyandry in a natural population, by using data from a long-term genetic and demographic study of lemon sharks (Negaprion brevirostris) at Bimini, Bahamas. To do so, we followed the fates of individuals from six cohorts (450 age-0 and 254 age-1 fish) in relation to their individual level of genetic variation, and whether they were from polyandrous or monoandrous litters. We find that offspring from polyandrous litters did not have a greater genetic diversity or greater survival than did the offspring of monoandrous litters. We also find no evidence of positive associations between individual offspring genetic diversity metrics and our surrogate measure of fitness (i.e. survival). In fact, age-1 individuals with fewer heterozygous microsatellite loci and more genetically similar parents were more likely to survive to age-2. Thus, polyandry in female lemon sharks does not appear to be adaptive from the perspective of indirect genetic benefits to offspring. It may instead be the result of convenience polyandry, whereby females mate multiply to avoid harassment by males. Our inability to find indirect genetic benefits of polyandry despite detailed pedigree and survival information suggests the need for similar assessments in other natural populations.

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.

On the resolution of the lek paradox

Directional female mate choice is expected to deplete additive genetic variation in male traits. This should preclude such trait-based choice from resulting in genetic benefits to offspring, and yet genetic benefits are the explanation for the choice. This evolutionary conundrum is known as the lek paradox. Newly proposed resolutions to this paradox aim to unravel mechanisms that contribute to the persistence of genetic variance in traits under directional female mate choice.

Symmetry and sexual dimorphism in human faces: interrelated preferences suggest both signal quality

Symmetry and masculinity in human faces have been proposed to be cues to the quality of the owner. Accordingly, symmetry is generally found attractive in male and female faces, and femininity is attractive in female faces. Women's preferences for male facial masculinity vary in ways that may maximize genetic benefits to women's offspring. Here we examine same- and opposite-sex preferences for both traits (Study 1) and intercorrelations between preferences for symmetry and sexual dimorphism in faces (Study 1 and Study 2) using computer-manipulated faces. For symmetry, we found that male and female judges preferred symmetric faces more when judging faces of the opposite-sex than when judging same-sex faces. A similar pattern was seen for sexual dimorphism (i.e., women preferred more masculine male faces than men did), but women also showed stronger preferences for femininity in female faces than men reported. This suggests that women are more concerned with female femininity than are men. We also found that in women, preferences for symmetry were positively correlated with preferences for masculinity in male faces and that in men preferences for symmetry were positively correlated with preferences for femininity in female faces. These latter findings suggest that symmetry and sexual dimorphism advertise a common quality in faces or that preferences for these facial cues are dependent on a common quality in the judges. Collectively, our findings support the view that preferences for symmetry and sexual dimorphism are related to mechanisms involved in sexual selection and mate choice rather than functionless by-products of other perceptual mechanisms.

Parasite levels in blue-black grassquits correlate with male displays but not female mate preference

The handicap principle proposes that male sexual ornaments and displays provide honest indicators of quality. Female preference for high-quality males, however, may be driven not only by genetic benefits but also by indirect benefits. We investigated the impact of parasitism on morphological, ornamental, and behavioral characteristics of male and female blue-black grassquits (Volatinia jacarina) in captivity. First, we tested whether male displays and morphology were influenced by parasitism. Second, we assessed if females were attentive to variation in male morphology and displays linked to parasitism. Third, we tested whether parasitism in females influenced health and mate preferences. We maintained 2 groups of birds in captivity: nonmedicated birds developed high levels of coccidian parasitism, whereas medicated birds were free of parasitism. Parasitized males developed, relative to nonparasitized males, lower weight/tarsus indices and mass. They also showed relative deficiencies in their displays, with less persistence and lower rates. Despite the negative effects of parasitism on males, females did not prefer nonparasitized males. This held for both parasitized and nonparasitized females. Our data suggest that coccidian parasitism has adverse effects on morphological condition and expression of displays. These effects, however, appear not to be attended to by females; moreover, female mate preferences appear not to be impacted by the threat of parasitism. It thus seems that female mate preferences may not depend only on sexual characters affected by parasitism in this species.

Short-term mating strategies and attraction to masculinity in point-light walkers

Strategic pluralism suggests that women engage in short-term sexual relationships when the benefits to doing so outweigh the costs. We investigated attraction to indicators of good genes (namely, masculinity as demonstrated by point-light walkers) in women varying in menstrual cycle status and sociosexual orientation. When women are fertile, they have the ability to gain genetic benefits from a male partner and should also be attracted to high levels of masculinity in men as a signal of genetic benefits. Sociosexual orientation is an individual difference that indicates openness to short-term mating and, thus, should influence aspects of mating strategy. Women with an unrestricted sociosexual orientation, as compared to women with a restricted sociosexual orientation, are more likely to engage in short-term relationships and obtain fewer nongenetic resources from their mates. Thus, they should place heavy emphasis on male masculinity as a sign of genetic benefits available from their mates. In this study, women indicated the walker most attractive to them on a constructed continuum of male and female point-light walkers. In Study 1, fertile women, as compared to nonfertile women, showed a greater attraction to masculinity. In Study 2, women demonstrated a strong positive relationship between sociosexuality and attraction to masculinity.

Do male ornaments signal immunity in the common yellowthroat?

Male ornaments may advertise genetic benefits to females choosing mates. These benefits may come in the form of genes for resistance to parasites and disease. Thus, females that prefer more ornamented males as mates may receive genes for enhanced immune system function for their offspring. The common yellowthroat (Geothlypis trichas) is the only species to date in which a male plumage ornament (size of the black facial mask) is known to be related to extrapair mating, and extrapair young are more immunocompetent than their within-pair half-sibs (at least in colder years). To investigate whether male mask size signals superior immune function, we examined male ornaments (mask and bib size and color) in relation to measures of overall health (hematocrit) and immune system function (plasma immunoglobulin G [IgG] concentration and cutaneous immune activity). We also investigated the role that testosterone may play in mediating the relationship between ornaments and immunity. Male mask size was correlated positively with IgG level, suggesting that male mask size may indicate humoral immunity. However, mask size was correlated negatively with hematocrit and cutaneous immune activity (our measure of nestling immunocompetence). Bib size and color were not related to these indices of immune function or health. Plasma testosterone level was neither related to immune function or health nor to the expression of male ornaments. These results suggest that there might be a trade-off between immune system components, as well as between immunity and the production or advertisement of male ornaments.

MULTIPLE GENETIC BENEFITS OF FEMALE PROMISCUITY IN A SOCIALLY MONOGAMOUS PASSERINE

The adaptive function of female extrapair mating in socially monogamous passerines is currently debated. In the bluethroat (Luscinia s. svecica), a previous study showed that offspring sired by extrapair males had a higher cell-mediated immunity than their within-pair half siblings, suggesting an immunogenetic benefit of extrapair mating in this species. Here, we expanded that dataset with two more years and investigated the association between extrapair paternity and microsatellite multilocus heterozygosity, in addition to cell-mediated immunity. We found that extrapair offspring were more heterozygous than their within-pair half siblings, and corroborated the previous finding of enhanced cellular immunity in extrapair offspring in this four-year dataset. The increased heterozygosity among extrapair offspring appeared to be a result of extrapair mates being less genetically similar than pair mates, and also less genetically similar than expected by random choice. Together with previous findings in this species, showing that the majority of females participate in extrapair copulations, our results indicate a postcopulatory cryptic female choice of genetically dissimilar males. The enhanced cellular immunity and increased heterozygosity were not related to each other, and hence our results indicate two independent genetic benefits of extrapair mating in the bluethroat.

Context-dependent genetic benefits of polyandry in a marine hermaphrodite.

Numerous studies emphasize the potential indirect (genetic) benefits of polyandry in animals with resource-free mating systems. In this paper, we examine the potential for these benefits to fuel sexual selection and polyandry in the hermaphroditic ascidian Pyura stolonifera. Individuals were designated either sire (sperm producers) or dam (egg producers) at random and crossed in a North Carolina II breeding design to produce both paternal and maternal half siblings for our quantitative genetic analysis. We then partitioned the phenotypic variance in fertilization and hatching rates into additive and non-additive variance components. We found significant additive variance attributable to sire and dam effects at fertilization and hatching, suggesting the potential for selection to favour individuals carrying intrinsically 'good genes' for these traits. In separate analyses involving monandrous and polyandrous clutches, we found that both traits were elevated under polyandry, but the difference in hatching rates was due entirely to the difference in fertilization rates between treatments. When the hatching rates were standardized to account for variance at fertilization, there was no overall net benefit of polyandry for this trait. Despite this, we found that hatching success declined with increasing embryo densities, and that the slope of this decline was significantly greater in monandrous than polyandrous clutches. Hence, selection on embryo viability may still favour polyandry under restricted environmental conditions. Nevertheless, our results caution against interpreting elevated hatching success as an indirect genetic benefit of polyandry when variance in fertilization is not controlled.