Paternal Variance Research Articles

Investigating the impact of paternal age, paternal heat stress, and estimation of non-genetic paternal variance on dairy cow phenotype

BackgroundLinear models that are commonly used to predict breeding values in livestock species consider paternal influence solely as a genetic effect. However, emerging evidence in several species suggests the potential effect of non-genetic semen-mediated paternal effects on offspring phenotype. This study contributes to such research by analyzing the extent of non-genetic paternal effects on the performance of Holstein, Montbéliarde, and Normande dairy cows. Insemination data, including semen Batch Identifier (BI, a combination of bull identification and collection date), was associated with various traits measured in cows born from the insemination. These traits encompassed stature, milk production (milk, fat, and protein yields), udder health (somatic cell score and clinical mastitis), and female fertility (conception rates of heifers and cows). We estimated (1) the effects of age at collection and heat stress during spermatogenesis, and (2) the variance components associated with BI or Weekly aggregated BI (WBI).ResultsOverall, the non-genetic paternal effect estimates were small and of limited biological importance. However, while heat stress during spermatogenesis did not show significant associations with any of the traits studied in daughters, we observed significant effects of bull age at semen collection on the udder health of daughters. Indeed, cows born from bulls collected after 1500 days of age had higher somatic cell scores compared to those born from bulls collected at a younger age (less than 400 days old) in both Holstein and Normande breeds (+ 3% and + 5% of the phenotypic mean, respectively). In addition, across all breeds and traits analyzed, the estimates of non-genetic paternal variance were consistently low, representing on average 0.13% and 0.09% of the phenotypic variance for BI and WBI, respectively (ranging from 0 to 0.7%). These estimates did not significantly differ from zero, except for milk production traits (milk, fat, and protein yields) in the Holstein breed and protein yield in the Montbéliarde breed when WBI was considered.ConclusionsOur findings indicate that non-genetic paternal information transmitted through semen does not substantially influence the offspring phenotype in dairy cattle breeds for routinely measured traits. This lack of substantial impact may be attributed to limited transmission or minimal exposure of elite bulls to adverse conditions.

Social group composition modulates the role of last male sperm precedence in post-copulatory sexual selection.

In many species, the order in which males mate with a female explains much of the variation in paternity arising from post-copulatory sexual selection. Research in Drosophila suggests that mating order may account for the majority of the variance in male reproductive success. However, the effects of mating order on paternity bias might not be static but could potentially vary with social or environmental factors. To test this idea, we used an existing dataset, collated from an experiment we previously published (Morimoto et al., PLoS One, 11, 2016, e0154468), with the addition of unpublished data from the same experiment. These previous experiments manipulated larval density in Drosophila melanogaster which generated variation in male and female body size, assembled groups of individuals of different sizes, and measured the mating success and paternity share of focal males. The data presented here provides information on each focal male's mating order and the frequency in which focal males remated with same females ('repetitive matings'). We combined this information with our previously reported focal male reproductive success to partition variance in paternity into male mating order and repetitive matings across groups that differed in the body size composition of males and females. We found, as expected, that male mating order explained a considerable portion of the variance in male paternity. However, we also found that the impact of male mating order on male paternity was influenced by the body size composition of groups. Specifically, males that tended to mate last had a greater paternity advantage, and displayed lower variance, in groups containing a heterogenous mixture male body sizes than in groups with a single male body size. Repetitive mating only had a minor contribution to the variance in male paternity share across all experiments. Overall, our findings contribute to the growing body of research showing that post-copulatory sexual selection is subject to socio-ecological influences.

Moving Beyond Access: Predictors of Maternity and Paternity Leave Duration in the United States

Parental leave has been linked to numerous positive child and family outcomes, yet little is known about which new mothers and fathers take longer parental leaves. Using structural equation modeling, we examined the financial, demographic, identity-relevant, and job characteristics that predict the duration of maternity and paternity leave in a community sample of 130 U.S. dual-earner couples who were followed across their transition to parenthood in 2008–2009. The findings show that financial characteristics, especially paid leave, are important for leave duration for both parents. In addition, identity-relevant and demographic characteristics mattered to length of paternity leave, whereas job characteristics were relevant to length of maternity leave. For fathers, longer leaves were associated with a greater proportion of paid leave, older paternal age, having a less planned pregnancy, and lower endorsement of maternal essentialism. For mothers, longer leaves were associated with a greater proportion of paid leave, higher household income, and lower job satisfaction. Together, these predictors explained 21% of the variance in maternity leave duration and 30% of the variance in paternity leave duration. In order for all U.S. parents, including fathers and low-income mothers, to reap the benefits of parental leave, financially incentivized leave would be most beneficial.

Factors influencing paternity in multiply mated female red-sided garter snakes and the persistent use of sperm stored over winter

In some species, sperm is stored within the female reproductive tract for months to years, and yet remains viable to fertilize eggs and produce offspring. Female red-sided garter snakes store sperm for over 7 months of winter dormancy. In previous work, we demonstrated that these stored sperm account for an average of 25 % paternity of a litter when the female mates with a male at spring emergence. Here, we tested whether last-male sperm precedence was prevalent when a female mates with two males during the spring. On average, paternity was shared equally among the first (P1 proportion of paternity of the first male to mate) and second males (P2) to mate in the spring, and stored sperm (Pss), but the variance in paternity was high. Thus, last male sperm precedence may diminish when a female has more than two mates. Male size did not affect paternity, but, as the interval between matings increased, P1 increased at the expense of Pss. Interestingly, as the second spring male’s copulation duration increased, P1 also increased at the expense of P2. This result suggests that female influence over sperm and/or copulatory plug transfer during matings may also affect which male fathers her offspring in response to coercive matings as we assisted females to mate for their second mating. Finally, all females were spring “virgins”; consequently, sperm stored from autumn matings (and/or previous spring matings) remain competitive even when faced with two rivals in sperm competition and is likely the driver of the evolution of sperm longevity.

Parental genetic distance and patterns in nonrandom mating and seed yield in predominately selfing Arabidopsis thaliana

In this study, we ask two questions: (1) Is reproductive success independent of parental genetic distance in predominately selfing plants? (2) In the absence of early inbreeding depression, is there substantial maternal and/or paternal variation in reproductive success in natural populations? Seed yield in single pollinations and proportion of seeds sired in mixed pollinations were studied in genetically defined accessions of the predominately selfing plant Arabidopsis thaliana by conducting two diallel crosses. The first diallel was a standard, single pollination design that we used to examine variance in seed yield. The second diallel was a mixed pollination design that utilized a standard pollen competitor to examine variance in proportion of seeds sired. We found no correlation between reproductive success and parental genetic distance, and self-pollen does not systematically differ in reproductive success compared to outcross pollen, suggesting that Arabidopsis populations do not experience embryo lethality due to early-acting inbreeding or outbreeding depression. We used these data to partition the contributions to total phenotypic variation from six sources, including maternal contributions, paternal contributions and parental interactions. For seed yield in single pollinations, maternal effects accounted for the most significant source of variance (16.6 %). For proportion of seeds sired in mixed pollinations, the most significant source of variance was paternal effects (17.9 %). Thus, we show that population-level genetic similarities, including selfing, do not correlate with reproductive success, yet there is still significant paternal variance under competition. This suggests two things. First, since these differences are unlikely due to early-acting inbreeding depression or differential pollen viability, this implicates natural variation in pollen germination and tube growth dynamics. Second, this strongly supports a model of fixation of pollen performance genes in populations, offering a focus for future genetic studies in differential reproductive success.

Parental genetic effects evaluation of growth-related traits of red common carp in China

Reciprocal differences have been observed widely for given traits in fish breeding programs, but maternal and paternal effects and heritable extranuclear genetic effects have often been omitted in the evaluation of genetic variance. In this study, we have applied a mixed genetic model to conduct a complete diallel cross using three varieties of red common carp (Cyprinus carpio L.), namely, C.carpio. var. singuonensis, C. carpio var. wuyuanensis and C.carpio var. color. Parental and direct (additive and dominance) genetic effects for growth-related traits at 8 and 20 months post-hatch were analyzed. At 8 months post-hatch, only significant additive and dominance variances were observed, while maternal and paternal variances were low and non-significant in the traits evaluated: body weight, total length, standard length, pre-dorsal height, pre-dorsal width, caudal peduncle length, and caudal peduncle height. At 20 months post-hatch, with the exception of significant additive and/or dominance variances, maternal variances were significant for the traits of body weight, pre-dorsal height, pre-dorsal width, and caudal peduncle height, and the paternal variance was significant only for total length. The maternal effects in the common carp had greater genetic influence on offspring than the paternal effects. Female C. carpio var. wuyuanensis were more suitable as brooders than males, but both female and male C. carpio var. color can be used as brooders according to breeding programs of improved traits. Cyprinus carpio var. singuonensis was the worst brooder of the three varieties of common carp evaluated.

The effect of sperm to egg ratio and gamete contact time on fertilization success in Atlantic cod Gadus morhua L.

Currently, Atlantic cod ( Gadus morhua) is the primary finfish species being developed for aquaculture in North Atlantic waters. Despite the importance of this species, no research has been conducted to assess the effects of sperm density and gamete contact time on egg fertilization. In two separate experiments male and female gametes were crossed using nested factorial designs. For each male–female combination we tested sperm to egg ratios ranging from 1 × 10 3:1 to 5 × 10 6:1. We also tested two gamete contact times where sperm and eggs were held in contact with each other for 5 or 30 min. Mixed-model ANOVAs indicated that sperm density and gamete contact time had a significant effect on fertilization success. Below a sperm to egg ratio of 1 × 10 5:1 fertilization success significantly decreased. Therefore, a standard sperm to egg ratio of 1 × 10 5 sperm per egg is recommended for fertilization in Atlantic cod. At the 1 × 10 3:1, 5 × 10 3:1, and 1 × 10 4:1 sperm to egg ratios maximum fertilization occurred after 30 min sperm to egg contact time. Gamete contact time was not significant at sperm to egg ratios of 1 × 10 5:1 and 1 × 10 6:1. Both the maternal and paternal variance components were significant for fertilization success. This information has important implications for optimizing family production in selective breeding programs, conserving sperm from superior pedigree in genome banks, maximizing the use of available gametes in hatchery or research facilities, and understanding mating success in the wild.

Parental and stock effects on larval growth and survival to metamorphosis in winter flounder ( Pseudopleuronectes americanus)

Geographically separated winter flounder ( Pseudopleuronectes americanus) populations in the northwest Atlantic Ocean are both phenotypically and genetically distinct from one another. This has important implications for winter flounder aquaculture with respect to broodstock selection; however, few studies have investigated the effect of population on larval growth and survival in a hatchery setting. In this study, eggs from Passamaquoddy Bay females were fertilized with sperm from Georges Bank and Passamaquoddy Bay males. Larvae were reared in common environmental conditions to evaluate population and parental contributions to variations in growth, and survival during early life history. Mixed-model nested ANOVAs revealed that larvae sired by Georges Bank males were significantly larger with respect to standard length, eye diameter, head depth, and jaw length during certain stages in larval development. Maternal, paternal, and parental interactions all contributed to morphological variation in developing larvae. Survival was strongly influenced by the paternal variance component. These results have two major implications: 1) they provide further supporting evidence that Georges Bank winter flounder are genetically selected for faster growth than larvae from inshore stocks, and 2) they suggest that aquaculture operations should also account for paternal variation so that the best broodstock can be selected for production.

Stock and parental effects on embryonic and early larval development of winter flounder Pseudopleuronectes americanus (Walbaum)

A hierarchical breeding design was used to determine if winter flounder Pseudopleuronectes americanus embryos and yolk‐sac larvae sired by Georges Bank males developed and grew larger than fish sired by Passamaquoddy Bay males, and to examine parental contributions to variations in fertilization success, time to 50% hatch, hatch success and larval morphological development. Significant stock effects were detected for time to hatch and larval development. Eggs fertilized by Passamaquoddy Bay males reached 50% hatch significantly earlier than eggs fertilized by Georges Bank males. Larvae sired by Georges Bank males were significantly larger during larval development for four of the six traits measured at 12 days post‐hatch: head depth, jaw length, myotome height and body area. Embryo and larval development were strongly influenced by maternal contributions; there were significant maternal variance components for the majority of the variables measured. Paternal variance components were significant for fertilization success, time to hatch, larval jaw length and larval head depth, however, they acted principally through parental interactions. This information has important implications for the long‐term sustainable development of winter flounder for aquaculture purposes as well as for understanding winter flounder genetic variation in the wild.

Sperm competition and evidence of sperm fertilization patterns in the carrion ball-roller beetle Canthon cyanellus cyanellus LeConte (Scarabaeidae: Scarabaeinae)

Field observation and laboratory experiments were conducted to investigate sperm competition and patterns of sperm fertilization under different experimental conditions in the carrion ball-roller beetle Canthon cyanellus cyanellus. Males in nature can mate with females whose spermathecae contains fertile sperm from other males. Sperm precedence was investigated using a visible genetic marker. The progeny of red (homozygous recessive) virgin females mated once with a red male and afterward, once with a green beetle (homozygous dominant) and vice versa, revealed that regardless of its color, the last male to mate fertilized c.a. 50% of the eggs, suggesting strong sperm competition. Males were able to achieve higher levels of paternity (more than 80%) when mated ad libitum with previously mated females, although large amount of variance in paternity does not exclude the possibility of first male sperm precedence or female cryptic choice. These results suggest that repeated mating and sperm replacement are the mechanisms by which last males achieve sperm precedence.

Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi.

Sexual conflict theory predicts an antagonistic coevolution, with each sex evolving adaptations and counter-adaptations to overcome a temporary dominance of the other sex over the control of paternity. Polyandry allows sexual selection to operate after mating has commenced, with male and female interests competing for control of fertilization. There are numerous examples of male control of paternity, but few studies have unambiguously revealed female control. Attributing variance in paternity to females is often difficult since male and female influences cannot be separated unambiguously. However, we show that polyandrous female orb-web spiders Argiope keserlingi (Arancidae) control the paternity of their offspring by adjusting the timing of sexual cannibalism. Our experiments reveal that females copulating with relatively smaller males delay sexual cannibalism, thereby prolonging the duration of copulation, and that these males consequently fertilize relatively more eggs.

Condition-dependent control of paternity by female purple martins: implications for coloniality

Proposed causal links between extra-pair copulation (EPC) and colony formation in socially monogamous birds hinge on the question of which sex controls fertilizations. We examined in colonial purple martins Progne subis (1) whether EPCs were forced or accepted by females, and (2) the degree to which apparently receptive females were able to obtain EPCs against their mates’ paternity defenses. Paternity analyses of multilocus DNA fingerprinting confirmed previous findings of a marked relationship between age class and extra-pair fertilizations (EPFs), with young males losing paternity of 43% (n = 53) of their putative offspring compared to 4% (n = 85) by old males. All assignable extra-pair offspring were sired by old males, with one male obtaining most EPFs each year. Contrary to the hypothesis that EPCs are forced, EPF frequency within age class did not increase with seasonal increases in the number of males per fertile female. Whereas the male control hypothesis predicted that the male age class that mate-guarded more would be cuckolded less, the reverse was true: young males guarded significantly more intensely. The male age class difference in cuckoldry could not be explained by the possibility that young and inexperienced females (which are usually paired to young males) were more vulnerable to forced copulation because EPFs were unrelated to female age. These findings suggest that females (1) pair with old males and avoid EPCs, or (2) pursue a mixed mating strategy of pairing with young males and accepting EPCs from old males. The receptivity to EPCs by females paired to young males put them in conflict with their mates. Two factors determined the paternity achieved by young males: (1) the relative size of the male to the female, with young males achieving much higher paternity when they were larger than their mates, and (2) the intensity of mate-guarding. Both variables together explained 77% of the variance in paternity and are each aspects of male-female conflict. Given female receptivity to EPCs, mate-guarding can be viewed as male interference with female mating strategies. We conclude that EPCs are rarely or never forced, but the opportunity for females paired to young males to obtain EPCs is relative to the ability of their mates to prevent them from encountering other males. Evidence of mixed mating strategies by females, combined with other features of the martin mating system, is consistent with the female-driven “hidden lek hypothesis” of colony formation which predicts that males are drawn to colonies when females seek extra-pair copulations.

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.