Bryan D. Neff

Genetic quality and sexual selection: an integrated framework for good genes and compatible genes

Why are females so choosy when it comes to mating? This question has puzzled and marveled evolutionary and behavioral ecologists for decades. In mating systems in which males provide direct benefits to the female or her offspring, such as food or shelter, the answer seems straightforward — females should prefer to mate with males that are able to provide more resources. The answer is less clear in other mating systems in which males provide no resources (other than sperm) to females. Theoretical models that account for the evolution of mate choice in such nonresource‐based mating systems require that females obtain a genetic benefit through increased offspring fitness from their choice. Empirical studies of nonresource‐based mating systems that are characterized by strong female choice for males with elaborate sexual traits (like the large tail of peacocks) suggest that additive genetic benefits can explain only a small percentage of the variation in fitness. Other research on genetic benefits has examined nonadditive effects as another source of genetic variation in fitness and a potential benefit to female mate choice. In this paper, we review the sexual selection literature on genetic quality to address five objectives. First, we attempt to provide an integrated framework for discussing genetic quality. We propose that the term ‘good gene’ be used exclusively to refer to additive genetic variation in fitness, ‘compatible gene’ be used to refer to nonadditive genetic variation in fitness, and ‘genetic quality’ be defined as the sum of the two effects. Second, we review empirical approaches used to calculate the effect size of genetic quality and discuss these approaches in the context of measuring benefits from good genes, compatible genes and both types of genes. Third, we discuss biological mechanisms for acquiring and promoting offspring genetic quality and categorize these into three stages during breeding: (i) precopulatory (mate choice); (ii) postcopulatory, prefertilization (sperm utilization); and (iii) postcopulatory, postfertilization (differential investment). Fourth, we present a verbal model of the effect of good genes sexual selection and compatible genes sexual selection on population genetic variation in fitness, and discuss the potential trade‐offs that might exist between mate choice for good genes and mate choice for compatible genes. Fifth, we discuss some future directions for research on genetic quality and sexual selection.

Multiple mating and sequential mate choice in guppies: females trade up.

The trade–up hypothesis outlines a behavioural strategy that females could use to maximize the genetic benefits to their offspring. The hypothesis proposes that females should be more willing to accept a mate when the new male encountered is a superior genetic source to previous mates. We provide a direct test of the trade–up hypothesis using guppies (Poecilia reticulata), and evaluate both behavioural and paternity data. Virgin female guppies were presented sequentially with two males of varying attractiveness, and their responsiveness to each male was quantified. Male attractiveness (ornamentation) was scored as the amount of orange coloration on their body. Females were generally less responsive to second–encountered males, yet responsiveness to second males was an increasing function of male ornamentation. These attractive second males also sired a greater proportion of the offspring. There was an overall tendency for last–male advantage in paternity, and this advantage was most exaggerated when the second male was more ornamented than the first. Finally, we found that our estimate of relative sperm number did not account for any significant variation in paternity. Our results suggest that female guppies may use pre–copulatory mechanisms to maximize the genetic quality of their offspring.

MICROSATELLITE EVOLUTION IN VERTEBRATES: INFERENCE FROM AC DINUCLEOTIDE REPEATS

Abstract We analyze published data from 592 AC microsatellite loci from 98 species in five vertebrate classes including fish, reptiles, amphibians, birds, and mammals. We use these data to address nine major questions about microsatellite evolution. First, we find that larger genomes do not have more microsatellite loci and therefore reject the hypothesis that microsatellites function primarily to package DNA into chromosomes. Second, we confirm that microsatellite loci are relatively rare in avian genomes, but reject the hypothesis that this is due to physical constraints imposed by flight. Third, we find that microsatellite variation differs among species within classes, possibly relating to population dynamics. Fourth, we reject the hypothesis that microsatellite structure (length, number of alleles, allele dispersion, range in allele sizes) differs between poikilotherms and homeotherms. The difference is found only in fish, which have longer microsatellites and more alleles than the other classes. Fifth, we find that the range in microsatellite allele size at a locus is largely due to the number of alleles and secondarily to allele dispersion. Sixth, length is a major factor influencing mutation rate. Seventh, there is a directional mutation toward an increase in microsatellite length. Eighth, at the species level, microsatellite and allozyme heterozygosity covary and therefore inferences based on large‐scale studies of allozyme variation may also reflect microsatellite genetic diversity. Finally, published microsatellite loci (isolated using conventional hybridization methods) provide a biased estimate of the actual mean repeat length of microsatellites in the genome.

Decisions about parental care in response to perceived paternity

Evolutionary ecologists are attempting to explain how parents make behavioural decisions about how much care to provide to their young. Theory predicts that when genetic relatedness to young is decreased by cuckoldry, for example, parents should reduce their care in favour of alternative broods that provide greater reproductive success. Experimental manipulation of perceived paternity has been used to test the theory, but such studies have generated mixed results. Some manipulations can fail to alter a parents perceived paternity, whereas others may directly affect parental behaviour when, for instance, the manipulation involves capturing the parent. No study has demonstrated parental care adjustment in a manner uncomplicated by experimental design or life history correlates. Here I test the theory using the fact that nest-tending parental male bluegill sunfish (Lepomis macrochirus) can assess their paternity using both the visual presence of parasitic cuckolder males during spawning, and olfactory cues released by newly hatched eggs. By manipulating both types of cues I show that parental males dynamically adjust their parental care, favouring broods that are apparently most closely related. These results confirm the importance of genetic relatedness in parental care decision-making.

Inter-population variation in multiple paternity and reproductive skew in the guppy.

We use microsatellite loci to detail the multiple paternity patterns in broods from 10 wild populations of the guppy (Poecilia reticulata) found in Northern Trinidad. The populations span two major drainages comprising the Caroni and the Oropouche, and include sites that are characterized by either high or low predation. Across the populations the frequency of multiple paternity is high with 95% (range: 70%–100%) of broods having multiple sires. Broods have an average of 3.5 sires (range: 1–9) and a mixed‐model analysis suggests that broods from high predation sites have marginally more sires than do those from low predation sites, but this is true only in the Oropouche drainage. There is no difference in sire number between predation sites in the Caroni drainage. Brood size, but not female body length, is correlated with the number of sires and the correlation cannot be attributed solely to the stochastic process associated with sperm competition and a ‘fair raffle’. Within broods there is significant skew in reproductive success among males, which may reflect variation in sperm competitiveness or female choice. There is, however, no difference in the skew among populations from different predation regimes or drainages. Finally, high predation populations were characterized by increased genetic variability at the microsatellite loci, suggesting a larger effective population size. We discuss explanations for the high degree of multiple paternity but the general lack of any major differences among broods from ecologically different populations.

MHC class IIB alleles contribute to both additive and nonadditive genetic effects on survival in Chinook salmon

The genes of the major histocompatibility complex (MHC) are found in all vertebrates and are an important component of individual fitness through their role in disease and pathogen resistance. These genes are among the most polymorphic in genomes and the mechanism that maintains the diversity has been actively debated with arguments for natural selection centering on either additive or nonadditive genetic effects. Here, we use a quantitative genetics breeding design to examine the genetic effects of MHC class IIB alleles on offspring survivorship in Chinook salmon (Oncorhynchus tshawytscha). We develop a novel genetic algorithm that can be used to assign values to specific alleles or genotypes. We use this genetic algorithm to show simultaneous additive and nonadditive effects of specific MHC class IIB alleles and genotypes on offspring survivorship. The additive effect supports the rare‐allele hypothesis as a potential mechanism for maintaining genetic diversity at the MHC. However, contrary to the overdominance hypothesis, the nonadditive effect led to underdominance at one heterozygous genotype, which could instead reduce variability at the MHC. Our algorithm is an advancement over traditional animal models that only partition variance in fitness to additive and nonadditive genetic effects, but do not allocate these effects to specific alleles and genotypes. Additionally, we found evidence of nonrandom segregation during meiosis in females that promotes an MHC allele that is associated with higher survivorship. Such nonrandom segregation could further reduce variability at the MHC and may explain why Chinook salmon has one of the lowest levels of MHC diversity of all vertebrates.

Dynamic adjustment of parental care in response to perceived paternity

Theories of parental care evolution predict that genetic relatedness will be an important variable in the amount of care a parent provides. However, current inferences of relatedness–based parental investment from studies in humans and birds remain challenged. No study has yet demonstrated parental care adjustment in a manner uncomplicated by life–history correlates or experimental design. We now present a unique test that controls for individual life histories and demonstrates paternity–related dynamic adjustments in parental care. Brood–rearing male bluegill sunfish (Lepomis macrochirus) that are cuckolded to a varying degree will either increase or decrease their parental investment in response to changing information on paternity during brood development. Specifically, as parental males detect paternity lost to cuckolders and, hence, a reduction in the value of their brood, they adaptively lower their level of parental care. Conversely, if they detect that their paternity is higher than previously assessed, they adaptively raise their level of parental care. This dynamic adjustment during brood rearing indicates the importance of genetic relatedness in parental investment decisions and provides needed empirical support for theoretical predictions.

Genetic quality and offspring performance in Chinook salmon: implications for supportive breeding

Each year salmon and other fishes are caught and used for supportive breeding programs that attempt to augment natural populations that are threatened with extinction. These programs typically mate individuals randomly and as such they overlook the importance of genetic quality to offspring fitness and ultimately to ensuring population health. Here, we use Chinook salmon (Oncorhynchus tshawytscha) and a fully crossed quantitative genetic breeding design to partition genetic variance in offspring performance (growth and survival) to additive and non-additive genetic effects as well as maternal effects. We show that these three effects contribute about equally to the variation in survival, but only non-additive genetic and maternal effects contribute to variation in growth. Some of the genetic effects could be assigned to variation at the class IIB locus of the major histocompatibility complex, but the maternal effects were not associated with egg size and we found no relationship between dam phenotypic measures and offspring survival or growth. We also found no relationship between sire sexually selected characters and offspring survival or growth, which is inconsistent with a “good genes” hypothesis. Finally, we show that incorporation of genetic quality into supportive breeding programs can increase offspring growth or survival by between 3% and 19% during the endogenous feeding stage alone, and projections to adulthood suggest that survivorship could be over four fold higher.

Relationships between condition factors, parasite load and paternity in bluegill sunfish, Lepomis macrochirus

Synopsis We examined the relationship between non-polar lipid density, parasite density and paternity of male bluegill sunfish, Lepomis macrochirus, and four condition factors: (1) Fultons condition factor, K; (2) the relative condition factor, K n ; (3) the relative mass index, W r ; and (4) the residuals from the geometric regression of mass on total length, C. Although the four factors were highly correlated to each other, only K and W r were significantly correlated with non-polar lipid density, explaining about 40% and 25% of the variation, respectively. K was also the best predictor of parasite density and was significantly correlated with the paternity of nesting males. These data provide support for K as a good indicator of individual energetic state and overall quality during the breeding period and demonstrate the importance of energetic state for understanding reproductive success in bluegill sunfish.

The MHC and non-random mating in a captive population of Chinook salmon

Detailed analysis of variation in reproductive success can provide an understanding of the selective pressures that drive the evolution of adaptations. Here, we use experimental spawning channels to assess phenotypic and genotypic correlates of reproductive success in Chinook salmon (Oncorhynchus tshawytscha). Groups of 36 fish in three different sex ratios (1:2, 1:1 and 2:1) were allowed to spawn and the offspring were collected after emergence from the gravel. Microsatellite genetic markers were used to assign parentage of each offspring, and the parents were also typed at the major histocompatibility class IIB locus (MHC). We found that large males, and males with brighter coloration and a more green/blue hue on their lateral integument sired more offspring, albeit only body size and brightness had independent effects. There was no similar relationship between these variables and female reproductive success. Furthermore, there was no effect of sex ratio on the strength or significance of any of the correlations. Females mated non-randomly at the MHC, appearing to select mates that produced offspring with greater genetic diversity as measured by amino-acid divergence. Females mated randomly with respect to male genetic relatedness and males mated randomly with respect to both MHC and genetic relatedness. These results indicate that sexual selection favours increased body size and perhaps integument coloration in males as well as increases genetic diversity at the MHC by female mate choice.