Parental Genetic Similarity Research Articles

How well do genetic markers inform about responses to intraspecific admixture? A comparative analysis of microsatellites and RADseq

BackgroundFitness consequences of intraspecific genetic admixture can vary from positive to negative depending on the genetic composition of the populations and environmental conditions. Because admixture has potential to influence the success of management and conservation efforts, genetic similarity has been suggested to be used as a proxy to predict the outcome. Studies utilizing microsatellites (a neutral marker) to investigate associations between genetic distance and admixture effects show conflicting results. Marker types that yield information on genome-wide and/or adaptive variation might be more useful for predicting responses to inter-population hybridization. In this study we utilized published data for three populations of pike (Esox lucius) to investigate associations between offspring performance (hatching success) and parental genetic similarity in experimentally purebred and admixed families, based on neutral (microsatellites), genome-wide neutral (RADseq SNPs), and adaptive (SNPs under selection) markers.ResultsEstimated similarity varied among the markers, likely reflecting differences in their inherent properties, but was consistently higher in purebred than admixed families. A significant interaction between marker type and admixture treatment reflected that neutral SNPs yielded higher estimates than adaptive SNPs for admixed families whereas no difference was found for purebred families, which indicates that neutral similarity was not reflective of adaptive similarity. When all samples were pooled, no association between similarity and performance was found for any marker. For microsatellites, similarity was positively correlated with hatching success in purebred families, whereas no association was found in admixed families; however, the direction of the effect differed between the population combinations.ConclusionsThe results strengthen the notion that, as of today, there is no proxy that can reliably predicted the outcome of admixture. This emphasizes the need of further studies to advance knowledge that can shed light on how to safeguard against negative consequences of admixture, and thereby inform management and promote conservation of biological diversity.

Evidence that genetic compatibility underpins female mate choice in a monandrous amphibian.

Mate choice for genetic benefits remains controversial, largely because few studies have estimated the relative contributions of additive and non-additive sources of genetic variation to offspring fitness. Moreover, there remains a deficit of these estimates for species where female-mate preferences have been quantified in the wild, especially species characterized by monandry or monogamy. Here, we use artificial fertilization techniques combined with a cross-classified breeding design to simultaneously test for "good genes" and "compatible genes" benefits of mate choice in the monandrous red backed toadlet (Pseudophryne coriacea). In addition, we used a genomic approach to estimate effects of parental-genetic relatedness (assessed using 27, 768 single nucleotide polymorphisms) on offspring fitness. Our results revealed no significant additive genetic effects (sire effects), but highly significant non-additive genetic effects (sire × dam interaction effects), on fertilization success, survival during embryonic development, and hatching success. We also found significant associations between parental genetic similarity and offspring survival (whereby survival was higher when parents were more related), and significant positive relationships between fertilization success and embryo survival through to hatching. These results indicate that offspring viability is significantly influenced by the genetic compatibility of parental genotypes, that more related parents are more genetically compatible, and that gametes with greater compatibility at fertilization produce more viable offspring. More broadly, our findings provide new quantitative genetic evidence that genetic incompatibility underpins female mate preferences. Continued quantitative genetic assessment of the relative importance of good genes versus compatible genes is needed to ascertain the general importance of genetic benefits as a driver of female mate choice.

Parental genetic similarity and offspring performance in blue tits in relation to brood size manipulation.

In birds, as in many other taxa, higher genetic similarity of mates has long been known to reduce offspring fitness. To date, the majority of avian studies have focused on examination whether the genetic similarity of social mates predicts hatching success. Yet, increased genetic similarity of mates may also reduce offspring fitness during later life stages, including the nestling period and beyond. Here, we investigated whether parental genetic similarity influences offspring performance using data from free‐living blue tits (Cyanistes caeruleus) collected across three breeding seasons. Additionally, we tested whether brood size manipulation affects the magnitude and direction of the relationship between genetic similarity of mates and offspring performance. Sixteen microsatellite markers were used to measure genetic similarity between biological parents. We found that the genetic similarity of parents negatively affects offspring immune response and this effect was independent of the experimental brood size manipulation.

Female choice for related males in wild red-backed toadlets (Pseudophryne coriacea)

AbstractMate choice for genetic benefits is assumed to be widespread in nature, yet very few studies have comprehensively examined relationships between female mate choice and male genetic quality in wild populations. Here, we use exhaustive sampling and single nucleotide polymorphisms to provide a partial test of the “good genes as heterozygosity” hypothesis and the “genetic compatibility” hypothesis in an entire population of terrestrial breeding red-backed toadlets, Pseudophryne coriacea. We found that successful males did not display higher heterozygosity, despite a positive relationship between male heterozygosity and offspring heterozygosity. Rather, in the larger of 2 breeding events, we found that successful males were more genetically similar to their mate than expected under random mating, indicating that females can use pre- or post-copulatory mate choice mechanisms to bias paternity toward more related males. These findings provide no support for the good genes as heterozygosity hypothesis but lend support to the genetic compatibility hypothesis. A complete test of this hypothesis will now require evaluating how parental genetic similarity impacts offspring fitness. Terrestrial toadlets show a high degree of site fidelity, high levels of genetic structuring between populations, and frequently hybridize with sister species. As such, female mate choice for related males may be an adaptive strategy to reduce outbreeding depression. Our findings provide the first population-wide evidence for non-random preferential inbreeding in a wild amphibian. We argue that such reproductive patterns may be common in amphibians because extreme genetic differentiation within meta-populations creates an inherently high risk of outbreeding depression.

Evidence of opposing fitness effects of parental heterozygosity and relatedness in a critically endangered marine turtle?

How individual genetic variability relates to fitness is important in understanding evolution and the processes affecting populations of conservation concern. Heterozygosity-fitness correlations (HFCs) have been widely used to study this link in wild populations, where key parameters that affect both variability and fitness, such as inbreeding, can be difficult to measure. We used estimates of parental heterozygosity and genetic similarity ('relatedness') derived from 32 microsatellite markers to explore the relationship between genetic variability and fitness in a population of the critically endangered hawksbill turtle, Eretmochelys imbricata. We found no effect of maternal MLH (multilocus heterozygosity) on clutch size or egg success rate, and no single-locus effects. However, we found effects of paternal MLH and parental relatedness on egg success rate that interacted in a way that may result in both positive and negative effects of genetic variability. Multicollinearity in these tests was within safe limits, and null simulations suggested that the effect was not an artefact of using paternal genotypes reconstructed from large samples of offspring. Our results could imply a tension between inbreeding and outbreeding depression in this system, which is biologically feasible in turtles: female-biased natal philopatry may elevate inbreeding risk and local adaptation, and both processes may be disrupted by male-biased dispersal. Although this conclusion should be treated with caution due to a lack of significant identity disequilibrium, our study shows the importance of considering both positive and negative effects when assessing how variation in genetic variability affects fitness in wild systems.

The consequences of mating over a range of parental genetic similarity in a selfing allopolyploid plant species

In diploids, F(1) offspring performance is expected to increase with increasing genetic dissimilarity between the parents until an optimum is reached because outbreeding mitigates inbreeding depression and maximizes heterosis. However, many flowering plant species are derived through allopolyploidization, i.e. interspecific hybridization with genome doubling. This mode of plant speciation can be expected to considerably alter the consequences of inbreeding and outbreeding. We investigated the F1 fitness consequences of mating over a range of (genetic) distances in the allohexaploid plant species Geum urbanum. Offspring was raised under controlled conditions (632 plants). The performance of outcrossed progeny was not significantly better than that of their selfed half-siblings and did not increase with parental genetic dissimilarity (0-0.83). Our findings support low, if any, inbreeding depression and heterosis. We attribute this to the peculiar state of quasi-permanent heterozygosity in allopolyploids and frequent selfing.

Complex selection associated with Hox genes in a natural population of lizards

Hox genes are recognized for their explanatory power of bilateral development. However, relatively little is known about natural variation in, and the evolutionary dynamics of, Hox genes within wild populations. Utilizing a natural population of sand lizards (Lacerta agilis), we screened HoxA13 for genetic variation and an association with incidence of offspring malformations. We found significant effects of parental genetic similarity and offspring sex, and their interaction, on risk of hatching malformed as an offspring. We also found within population genetic variation in HoxA13, and identified a significant effect of a three-way interaction among Hox genotype, parental genetic similarity, and offspring sex on the risk of hatching malformation. Since malformed offspring in this population do not survive to maturity, this study reveals complex and ongoing selection associated with Hox genes in a wild reptile population. Importantly, this demonstrates the utility of natural populations in unveiling microevolutionary processes shaping variation in highly conserved genes.

Females may not obtain indirect genetic benefits from extra-pair paternity in vinous-throated parrotbills, Paradoxornis webbianus

In birds, determining what females seek through extra-pair paternity (EPP) is fundamental in the understanding of variation in the incidence of EPP within and between species. I conducted genetic parentage analyses in vinous-throated parrotbills, Paradoxornis webbianus, a typical double-brooded passerine with a strong flock habit. In this species, it is known that the prevalence of EPP varies significantly between two egg-laying peaks; 95% of EPP occurred in the first peak. In the present study, I focused on whether or not females obtain genetic benefits through EPP and its relevance to the biased distribution of EPP between the two laying peaks. I found that females did not obtain ‘good genes’ so that extra-pair young were not better than within-pair young in terms of their body condition at the nestling stage or their survival rate to their first winter. I also found no significant effect of parental genetic similarity and local genetic diversity on the occurrence of EPP, and these genetic correlates were not related to the patchy distribution of EPP. Overall, this study concluded that female parrotbills may not pursue indirect benefits through EPP, and further study testing the possibility of direct benefits will be worthwhile.

Temporal dynamics of genetic variability in a mountain goat (Oreamnos americanus) population

The association between population dynamics and genetic variability is of fundamental importance for both evolutionary and conservation biology. We combined long-term population monitoring and molecular genetic data from 123 offspring and their parents at 28 microsatellite loci to investigate changes in genetic diversity over 14 cohorts in a small and relatively isolated population of mountain goats (Oreamnos americanus) during a period of demographic increase. Offspring heterozygosity decreased while parental genetic similarity and inbreeding coefficients (F(IS) ) increased over the study period (1995-2008). Immigrants introduced three novel alleles into the population and matings between residents and immigrants produced more heterozygous offspring than local crosses, suggesting that immigration can increase population genetic variability. The population experienced genetic drift over the study period, reflected by a reduced allelic richness over time and an 'isolation-by-time' pattern of genetic structure. The temporal decline of individual genetic diversity despite increasing population size probably resulted from a combination of genetic drift due to small effective population size, inbreeding and insufficient counterbalancing by immigration. This study highlights the importance of long-term genetic monitoring to understand how demographic processes influence temporal changes of genetic diversity in long-lived organisms.

Paternal Song Complexity Predicts Offspring Sex Ratios Close to Fledging, but not Hatching, in Song Sparrows

Abstract Sex allocation theory predicts that population sex ratios should be generally stable and close to unity, but individuals may benefit by adjusting the sex ratio of their offspring. For example, females paired with attractive males may benefit by overproducing sons relative to daughters, as sons inherit their fathers' attractive ornaments (“sexy son” hypothesis). Similarly, if compatible gene effects on fitness are more pronounced in males than females, genetically dissimilar mated pairs may enhance fitness by overproducing sons (“outbred son” hypothesis). We tested these hypotheses in Song Sparrows (Melospiza melodia) by examining offspring sex ratios of 64 complete families shortly after hatching (“early-stage”) and again shortly before fledging (“late-stage”) in relation to paternal song complexity and the genetic similarity of social mates. Neither early nor late-stage offspring sex ratio was related to parental genetic similarity. Nests of males with larger song repertoires contained more male...

Biparental inbreeding depression, genetic relatedness and progeny vigour in a wind-pollinated treeline species in Argentina

Spatially restricted gene flow and resulting spatial genetic structure are generally considered as being the primary controlling factors in the dynamics of biparental inbreeding depression in a wide range of plant species. However, wind-pollinated angiosperm trees have not been studied adequately in this respect. The present study analyses the relationships among parental genetic similarity, outcrossing distances, progeny vigour and mortality in Polylepis australis (Rosaceae), a wind-pollinated treeline species endemic to Argentina. We investigated whether spatial genetic structuring occurs in anthropogenically fragmented P. australis woodlands of the Córdoba Mountains. We also performed a controlled crossing experiment using pollen collected from different distances. Genetic variability (using RAPD-PCR), vigour (N-metabolism capacity) and mortality of the resulting progeny were contrasted with progeny from unmanipulated flowers. We found a continuous decrease in parental genetic similarity with spatial distance among mates and an increase in N-metabolism capacity in the progeny produced from pollen at increasing distances, as well as a very high mortality of seedlings resulting from short-distance crosses. Additionally, our results suggest that there is still fragment connectivity in P. australis through long-distance pollen-mediated gene flow.

Genetic similarity of mates, offspring health and extrapair fertilization in house sparrows

High genetic similarity or dissimilarity between parents may result in viability consequences for offspring. However, because female choice of a social mate often reflects access to resources or male parental care, optimal genetic complementarity may be unattainable for social pairs. Thus, extrapair copulations may serve to increase offspring viability by allowing females to obtain sperm from males with more compatible genomes than those of social mates. We investigated whether parental genetic similarity influences offspring viability, including immunocompetence, in house sparrows, Passer domesticus. We also explored whether genetic similarity of social mates predicts the prevalence of young sired through extrapair fertilizations, and whether females enhance offspring viability by engaging in extrapair matings. We used DNA fingerprinting to estimate genetic similarity between social mates, and we assessed offspring viability using two measures of nestling immune response, the phytohaemagglutinin skin test and heterophil:lymphocyte ratios, plus nestling body mass and hatching success. We found no associations between the genetic similarity of parents and offspring immunocompetence, mass or hatching success; however, parental genetic similarity was positively correlated with clutch size. Genetic similarity of social mates also did not predict the frequency of extrapair young. Furthermore, maternal half-siblings within broods of mixed paternity did not differ in immunocompetence. Thus, our results provide no evidence for enhancement of offspring viability as an incentive for female engagement in extrapair copulations.

Genomic compatibility occurs over a wide range of parental genetic similarity in an outcrossing plant

The theory of inbreeding and outbreeding suggests that there is a hump-shaped relationship between the genetic similarity of sexually reproducing parents and the performance of their offspring. Inbreeding depression occurs when genetic similarity is high, whereas hybrid breakdown is expected when genetic similarity is low. Between these extremes, the effect of genetic similarity on fitness is unclear. We studied the shape of this relationship by crossing 65 target genotypes of the clonal, self-incompatible Ranunculus reptans with partner genotypes spanning a broad scale of genetic similarity, ranging from crosses within populations to between-population crosses and hybridisation with a closely related species. Offspring were raised in outdoor tubs. Results revealed a quadratic relationship between parental genetic distance and offspring performance, with the clonal component of fitness more strongly hump-shaped than the sexual component. Optimal genetic similarity encompassed a broad range of within-population and between-population crosses. This pattern of genomic compatibility has important implications for the evolution of mating systems and mate choice.

Parental genetic characteristics and hatching success in the spotless starling, Sturnus unicolor

Several studies have shown that inbreeding causes low hatching success. However, it is not always clear under which parental genetic characteristics hatching failure occurs. We examined the effects of parental homozygosity and parental genetic similarity on egg hatchability in the spotless starling. We evaluated whether low hatchability was a consequence of genetic similarity of the parents producing a zygote or because the parents themselves had reduced fertility because of their own genetic characteristics. We found a significant detrimental effect of both highest and lowest female homozygosity on hatchability. Parental genetic similarity was negatively related to egg hatchability. In contrast, we found no significant effect of male homozygosity on hatching success. Our results suggest that effects of homozygosity on hatching success may be relevant even in populations of abundant and colonial wild bird species without geographical barriers that could limit immigration or dispersal. We also highlight the importance of the analyses of male and female homozygosity and parental genetic similarity when investigating related fitness consequences of inbreeding.

SEED SET AND SEED MASS IN IPOMOPSIS AGGREGATA: VARIANCE PARTITIONING AND INFERENCES ABOUT POSTPOLLINATION SELECTION.

Events that follow pollination, such as pollen-tube growth and seed maturation, comprise an important phase of angiosperm reproduction. Differential success during this "postpollination" phase may represent phenotypic selection, including sexual selection, or interaction between parents caused, for example, by their genetic similarity. By providing a detailed partitioning of variance in success, diallel crossing designs offer great potential to determine which processes are occurring and their relative magnitudes. We performed three partial diallels with the montane herb Ipomopsis aggregata, using a large sample of parental plants (69 total). Embedded in the designs were crossing-distance treatments of 1 m, 10 m, and 100 m, reflecting a range of parental genetic similarity. We partitioned phenotypic variance in seed set per fruit into six components using restricted maximum-likelihood (REML) analysis. For one diallel, we also partitioned variance in seed mass into five components, and estimated two components of covariance between seed set and mass. Variance caused by maternal effects (Vmat ) comprised 12%-35% of total variance in seed set and 62% of variance in seed mass, and there was a significant negative environmental covariance between seed set and seed mass. Parental interaction made no detectable contribution to phenotypic variance in either of our measures of postpollination success, although crossing distance did contribute slightly but significantly to fit of the model in some cases. Finally, there was no detectable paternal variance (Vpat ) in seed set or seed mass. These results are in keeping with reports from other studies of natural plant populations. The finding of little or no paternal variance in particular suggests little scope for postpollination sexual selection through the male function of cosexual plants such as I. aggregata.

Crossing Distance Effects on Prezygotic Performance in Plants: An Argument for Female Choice

Seed set in the perennial larkspur Delphinium nelsonii is greater in crosses between plants growing an intermediate distance apart than in shorter and longer crosses. Since crossing distance is an attribute of a specific combination of parents, its effect on seed set represents an interaction of these parents, and since genetic similarity declines with physical distance in D. nelsonii populations, the interaction reflects parental genetic similarity. Understanding processes responsible for the effect is simplified if seed set differences result from prezygotic events, because in this case no inbreeding or outbreeding depression are involved. In 1990 we observed pollen tubes after performing crosses between plants separated by 1 m, 10 m, or 100 m, and found that the intermediate, 10 m crosses delivered the most tubes to the ovary