Sex differences in life history drive evolutionary transitions among maternal,paternal, and bi‐parental care

Evolutionary transitions among maternal, paternal, and bi‐parental care have been common in many animal groups. We use a mathematical model to examine the effect of male and female life‐history characteristics (stage‐specific maturation and mortality) on evolutionary transitions among maternal, paternal, and bi‐parental care. When males and females are relatively similar – that is, when females initially invest relatively little into eggs and both sexes have similar mortality and maturation – transitions among different patterns of care are unlikely to be strongly favored. As males and females become more different, transitions are more likely. If females initially invest heavily into eggs and this reduces their expected future reproductive success, transitions to increased maternal care (paternal → maternal, paternal → bi‐parental, bi‐parental → maternal) are favored. This effect of anisogamy (i.e., the fact that females initially invest more into each individual zygote than males) might help explain the predominance of maternal care in nature and differs from previous work that found no effect of anisogamy on the origin of different sex‐specific patterns of care from an ancestral state of no care. When male mortality is high or male egg maturation rate is low, males have reduced future reproductive potential and transitions to increased paternal care (maternal → paternal, bi‐parental → paternal, maternal → bi‐parental) are favored. Offspring need (i.e., low offspring survival in the absence of care) also plays a role in transitions to paternal care. In general, basic life‐history differences between the sexes can drive evolutionary transitions among different sex‐specific patterns of care. The finding that simple life‐history differences can alone lead to transitions among maternal and paternal care suggests that the effect of inter‐sexual life‐history differences should be considered as a baseline scenario when attempting to understand how other factors (mate availability, sex differences in the costs of competing for mates) influence the evolution of parental care.     

The origin of parental care in relation to male and female life history

The evolution of maternal, paternal, and bi‐parental care has been the focus of a great deal of research. Males and females vary in basic life‐history characteristics (e.g., stage‐specific mortality, maturation) in ways that are unrelated to parental investment. Surprisingly, few studies have examined the effect of this variation in male and female life history on the evolution of care. Here, we use a theoretical approach to determine the sex‐specific life‐history characteristics that give rise to the origin of paternal, maternal, or bi‐parental care from an ancestral state of no care. Females initially invest more into each egg than males. Despite this inherent difference between the sexes, paternal, maternal, and bi‐parental care are equally likely when males and females are otherwise similar. Thus, sex differences in initial zygotic investment do not explain the origin of one pattern of care over another. However, sex differences in adult mortality, egg maturation rate, and juvenile survival affect the pattern of care that will be most likely to evolve. Maternal care is more likely if female adult mortality is high, whereas paternal care is more likely if male adult mortality is high. These findings suggest that basic life‐history differences between the sexes can alone explain the origin of maternal, paternal, and bi‐parental care. As a result, the influence of life‐history characteristics should be considered as a baseline scenario in studies examining the origin of care.     

The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae)

Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.     

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.     

Links between parental life histories of wild salmon and the telomere lengths of their offspring

The importance of parental contributions to offspring development and subsequent performance is self‐evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e., telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, although the effects of other parental contribution pathways have been far less studied. Using wild Atlantic salmon with different parental life histories in an experimental split‐brood in vitro fertilization mating design and rearing the resulting families under standardized conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life.     

Maternal influence on plasma cholesterol variation.

Evidence for maternal effects on plasma cholesterol was found by comparing the variance between maternal and paternal half siblings obtained from 83 families of monozygotic twin pairs (424 children). Maternal effects accounted for about one-fifth of the total variance.     

Parental height differences predict the need for an emergency caesarean section

More than 30% of all pregnancies in the UK require some form of assistance at delivery, with one of the more severe forms of assistance being an emergency Caesarean section (ECS). Previously it has been shown that the likelihood of a delivery via ECS is positively associated with the birth weight and size of the newborn and negatively with maternal height. Paternal height affects skeletal growth and mass of the fetus, and thus might also affect pregnancy outcomes. We hypothesized that the effect of newborn birth weight on the risk of ECS would decrease with increasing maternal height. Similarly, we predicted that there would be an increase in ECS risk as a function of paternal height, but that this effect would be relative to maternal height (i.e., parental height differences). We used data from the Millennium Cohort Study: a large-scale survey (N = 18,819 births) with data on babies born and their parents from the United Kingdom surveyed 9 to 12-months after birth. We found that in primiparous women, both maternal height and parental height differences interacted with birth weight and predicted the likelihood of an ECS. When carrying a heavy newborn, the risk of ECS was more than doubled for short women (46.3%) compared to tall women (21.7%), in agreement with earlier findings. For women of average height carrying a heavy newborn while having a relatively short compared to tall partner reduced the risk by 6.7%. In conclusion, the size of the baby, the height of the mother and parental height differences affect the likelihood of an ECS in primiparous women.     

No paternal effect on monozygotic twinning in the Swedish Twin Registry.

Previous research has provided evidence for a genetic effect in monozygotic twinning, indicated by an increased risk for monozygotic women to have monozygotic offspring. However, since the biological mechanism for this trait is unknown, it is not clear if there exists a paternal inheritance. In this study we investigated twin pregnancies in offspring born in 1941-1996 to male twins in the Swedish Twin Registry and population controls born in 1926-1980. In total 4,225,331 offspring, of which 89,286 were twins, were studied. There was neither an increase in the probability for monozygotic men to have like-sexed twin offspring risk ratio (RR = 0.95; 95% CI = 0.77-1.13) nor an increase in the estimated number of monozygotic twin births. Thus, there is no evidence for a paternal effect on monozygotic twinning, suggesting that the gene(s) increasing the liability for division of the embryo are expressed in the mother and not in the fertilised egg.     

The General Factor of Personality (GFP) and parental support: testing a prediction from Life History Theory

In the present study, we tested whether the General Factor of Personality (GFP) is related to the level of parental support. The GFP is assumed to occupy the apex of the hierarchy of human personality structure and is believed to reflect a socially and sexually selected aggregate of behavioral characteristics that are generally valued as “desirable” in interpersonal relationships. The relationship between the GFP and parental support tested in this study is predicted by Life History Theory, a midlevel evolutionary account of systematic differences in evolved reproductive strategies. A total of 428 families with mother, father, and two children (range 14–16 years) participated. Parents filled out personality questionnaires (Big Five) and their level of parental support. The children also independently rated the amount of support they perceived from their parents. In the present sample, parents' GFPs were found to explain 33% of the variance in the Big Five. Moreover, the parents' GFPs showed significant relationships with the parents' self-rated parental support, but also with the child-rated parental support. The monoinformant (parents ratings) and multi-informant (parent and child ratings) data support the notion of a substantive GFP that is related to the investment of parents into their offspring.     

The relative importance of genetic and nongenetic inheritance in relation to trait plasticity in Callosobruchus maculatus

A trait's response to natural selection will reflect the nature of the inheritance mechanisms that mediate the transmission of variation across generations. The relative importance of genetic and nongenetic mechanisms of inheritance is predicted to be related to the degree of trait plasticity, with nongenetic inheritance playing a greater role in the cross‐generational transmission of more plastic traits. However, this prediction has never been tested. We investigated the influence of genetic effects and nongenetic parental effects in two morphological traits differing in degree of plasticity by manipulating larval diet quality within a cross‐generational split‐brood experiment using the seed beetle Callososbuchus maculatus. In line with predictions, we found that the more plastic trait (elytron length) is strongly influenced by both maternal and paternal effects whereas genetic variance is undetectable. In contrast, the less plastic trait (first abdominal sternite length) is not influenced by parental effects but exhibits abundant genetic variance. Our findings support the hypothesis that environment‐dependent parental effects may play a particularly important role in highly plastic traits and thereby affect the evolutionary response of such traits.     

New chromosome 11p15 epigenotypes identified in male monozygotic twins with Beckwith-Wiedemann syndrome

Beckwith-Wiedemann syndrome (BWS) is an overgrowth syndrome demonstrating heterogeneous molecular alterations of two imprinted domains on chromosome 11p15. The most common molecular alterations include loss of methylation at the proximal imprinting center, IC2, paternal uniparental disomy (UPD) of chromosome 11p15 and hypermethylation at the distal imprinting center, IC1. An increased incidence of female monozygotic twins discordant for BWS has been reported. The molecular basis for eleven such female twin pairs has been demonstrated to be a loss of methylation at IC2, whereas only one male monozygotic twin pair has been reported with this molecular defect. We report here two new pairs of male monozygotic twins. One pair is discordant for BWS; the affected twin exhibits paternal UPD for chromosome 11p15 whereas the unaffected twin does not. The second male twin pair is concordant for BWS and both twins of the pair demonstrate hypermethylation at IC1. Thus, this report expands the known molecular etiologies for BWS twins. Interestingly, these findings demonstrate a new epigenotype-phenotype correlation in BWS twins. That is, while female monozygotic twins with BWS are likely to show loss of imprinting at IC2, male monozygotic twins with BWS reflect the molecular heterogeneity seen in BWS singletons. These data underscore the need for molecular testing in BWS twins, especially in view of the known differences among 11p15 epigenotypes with respect to tumor risk.     

Sensitive flow cytometric analysis reveals a novel type of parent-of-origin effect in the mouse genome

The discovery of classic parental imprinting came, at least in part, from the analysis of transgene expression in mice. It was noticed that some transgenes were only expressed following paternal transmission and that others sometimes showed differential patterns of methylation depending on the parent of origin. Here, we present evidence of a novel and more subtle form of parental imprinting by taking advantage of the highly sensitive detection of murine transgene expression afforded by flow cytometry. We have produced nine lines of transgenic mice carrying a GFP reporter linked to the human alpha-globin promoter and enhancer elements, which direct expression to erythroid cells. A high proportion of transgenic lines, four of the nine, display significantly lower levels of expression following maternal transmission. Both the percentage of expressing cells and the mean fluorescence in expressing cells are between 10% and 30% lower following maternal transmission. These effects are reversible upon passage through the opposite germline. This finding raises the possibility that differences in the epigenetic state of the maternal and paternal chromosomes in adult somatic cells are more widespread than was previously thought.     

Genetic and maternal influences on life history plasticity in milkweed bugs (Oncopeltus): response to temperature

This study was designed to examine life history flexibility arising from phenotypic plasticity in response to temperature and from maternal effects in response to reproductive diapause in a temperate zone population of the milkweek bug (Oncopeltus fasciatus). We employed a split-family, first-cousin, full-sib design with siblings reared at different temperatures in order to quantify phenotypic plasticity, maternal effects, and variation for each. The following traits were analyzed: development time, age at first reproduction, longevity, early-life fecundity, and wing length. We found both life history plasticity and maternal effects on life history traits which tend to enhance the colonizing ability of offspring born to mothers that have undergone reproductive diapause. We were unable to demonstrate additive genetic variation for plasticity for any of the traits, while for development time and wing length we found variation due to non-additive genetic or common-environmental sources. We were also unable to demonstrate additive genetic variation for maternal effects, although variation may exist at low levels that are difficult to detect using cousin-families. The apparent lack of variation in this population would constrain evolution of life history flexibility even though considerable flexibility exists in the phenotype.     

A search for a paternal-age effect upon cases of 47, +21 in which the extra chromosome is of paternal origin

If there is a paternal-age effect for 47, +21, it would appear most likely to be present primarily, if not exclusively, in cases in which the extra chromosome is of paternal origin. To search for such an effect, data were reviewed from seven series reporting at least four cases of 47, +21 of paternal origin. The mean of the paternal age-maternal-age difference of such cases (dp) in each series was compared with the mean of the paternal-age differences of cases in the same series that were of maternal origin (dm). If the difference between these (dp - dm or delta) is greater than zero, then this would imply a positive paternal-age effect among cases of paternal origin, at least compared to those of maternal origin. In the seven series, the values of delta ranged from -2.2 years to +3.4 years, and there was no evidence in these comparisons for any consistent trend. A second analysis controlled for any effect of maternal-age variation upon this difference. Each case of paternal origin was matched with a case of maternal origin in the same series that was of the same maternal age. Of 60 cases of paternal origin, exact matches were found for 38. In these 38, the mean value of the difference in parental ages, dp - dm or delta, was negative, about -1.1 (+/- 5.1 years). The difference was highest for the nine cases of paternal origin in which the extra chromosome resulted from presumptive second-division non-disjunction, -1.8 (+/- 3.8 years).(ABSTRACT TRUNCATED AT 250 WORDS)     

The personalities of twins: just ordinary folks.

Twin studies have demonstrated that personality traits show moderate genetic influence. The conclusions drawn from twin studies rely on the assumptions that twins are representative of the population at large and that monozygotic and dizygotic twins are comparable in every way that might have bearing on the traits being studied. To evaluate these assumptions, we used Multidimensional Personality Questionnaire (MPQ) data from three samples drawn from the Minnesota Twin Registry (totaling 12,971 respondents) to examine the effect sizes associated with mean differences on the 11 MPQ scales and 3 higher-order MPQ factors for singletons versus twins and MZ twins versus DZ twins. The singletons in the samples were family members of the participating twins. We also used ratios of scale variances to examine the significance of variance differences. The only mean or variance difference replicated across all three samples was greater Social Closeness (about.1 standard deviation) for twins than for singletons. This difference was obtained for both males and females. It would appear that, with respect to personality, twins are not systematically different from other people. Our results also highlight the importance of replication in psychological research because each of our large samples showed differences not replicated in other samples.     

EFFECTS OF MATERNAL AND PATERNAL ENVIRONMENT AND GENOTYPE ON OFFSPRING PHENOTYPE IN SOLIDAGO ALTISSIMA L.

To predict the possible evolutionary response of a plant species to a new environment, it is necessary to separate genetic from environmental sources of phenotypic variation. In a case study of the invader Solidago altissima, the influences of several kinds of parental effects and of direct inheritance and environment on offspring phenotype were separated. Fifteen genotypes were crossed in three 5 × 5 diallels excluding selfs. Clonal replicates of the parental genotypes were grown in two environments such that each diallel could be made with maternal/paternal plants from sand/sand, sand/soil, soil/sand, and soil/soil. In a first experiment (1989) offspring were raised in the experimental garden and in a second experiment (1990) in the glasshouse. Parent plants growing in sand invested less biomass in inflorescences but produced larger seeds than parent plants growing in soil. In the garden experiment, phenotypic variation among offspring was greatly influenced by environmental heterogeneity. Direct genetic variation (within diallels) was found only for leaf characters and total leaf mass. Germination probability and early seedling mass were significantly affected by phenotypic differences among maternal plants because of genotype ( genetic maternal effects ) and soil environment ( general environmental maternal effects ). Seeds from maternal plants in sand germinated better and produced bigger seedlings than seeds from maternal plants in soil. They also grew taller with time, probably because competition accentuated the initial differences. Height growth and stem mass at harvest (an integrated account of individual growth history) of offspring varied significantly among crosses within parental combinations ( specific environmental maternal effects ). In the glasshouse experiment, the influence of environmental heterogeneity and competition could be kept low. Except for early characters, the influence of direct genetic variation was large but again leaf characters (= basic module morphology) seemed to be under stricter genetic control than did size characters. Genetic maternal effects, general environmental maternal effects, and specific environmental maternal effects dominated in early characters. The maternal effects were exerted both via seed mass and directly on characters of young offspring. Persistent effects of the general paternal environment ( general environmental paternal effects ) were found for leaf length and stem and leaf mass at harvest. They were opposite in direction to the general environmental maternal effects, that is the same genotypes produced “better mothers” in sand but “better fathers” in soil. The general environmental paternal effects must have been due to differences in pollen quality, resulting from pollen selection within the male parent or leading to pre- or postzygotic selection within the female parent. The ranking of crosses according to mean offspring phenotypes was different in the two experiments, suggesting strong interaction of the observed effects with the environment. The correlation structure among characters changed less between experiments than did the pattern of variation of single characters, but under the competitive conditions in the garden plant height seemed to be more directly related to fitness than in the glasshouse. Reduced competition could also explain why maternal effects were less persistent in the glasshouse than in the garden experiment. Evolution via selection of maternal effects would be possible in the study population because these effects are in part due to genetic differences among parents.     

Sex allocation in the sexually monomorphic fairy martin

Offspring sex ratios were examined at the population and family level in the sexually monomorphic, socially monogamous fairy martin Petrochelidon ariel at five colony sites over a 4-year period (1993–1996). The sex of 465 nestlings from 169 broods was determined using sex-specific PCR at the CHD locus. In accordance with predicted sex allocation patterns, population sex ratios at hatching and fledging did not differ from parity in any year and the variance in brood sex ratios did not deviate from the binomial distribution. Further, brood sex ratio did not vary with hatching date during the season, brood number, brood size or colony size. The sex ratio of broods with extra-pair young did not differ from those without, while the sex ratio of broods fathered by males that gained extra-pair fertilizations did not differ from broods fathered by other males. Extra-pair chicks were as likely to be male as female. Neither the total number of feeding visits to the brood nor the relative feeding contribution by the sexes varied significantly with brood sex ratio. Brood sex ratios were also unrelated to paternal size, condition and breeding experience or maternal condition and breeding experience. However, contrary to our prediction, brood sex ratio was negatively correlated with maternal size. Generally, these results were consistent with our expectations that brood sex ratios would not vary with environmental factors or parental characteristics, and would not influence the level of parental provisioning. However, the finding that females with longer tarsi produced an excess of daughters is difficult to reconcile with our current understanding of fairy martin life history and breeding ecology.     

Transgenerational effects of nutrition are different for sons and daughters

Food shortage is an important selective factor shaping animal life‐history trajectories. Yet, despite its role, many aspects of the interaction between parental and offspring food environments remain unclear. In this study, we measured developmental plasticity in response to food availability over two generations and tested the relative contribution of paternal and maternal food availability to the performance of offspring reared under matched and mismatched food environments. We applied a cross‐generational split‐brood design using the springtail Orchesella cincta, which is found in the litter layer of temperate forests. The results show adverse effects of food limitation on several life‐history traits and reproductive performance of both parental sexes. Food conditions of both parents contributed to the offspring phenotypic variation, providing evidence for transgenerational effects of diet. Parental diet influenced sons’ age at maturity and daughters’ weight at maturity. Specifically, being born to food‐restricted parents allowed offspring to alleviate the adverse effects of food limitation, without reducing their performance under well‐fed conditions. Thus, parents raised on a poor diet primed their offspring for a more efficient resource use. However, a mismatch between maternal and offspring food environments generated sex‐specific adverse effects: female offspring born to well‐fed mothers showed a decreased flexibility to deal with low‐food conditions. Notably, these maternal effects of food availability were not observed in the sons. Finally, we found that the relationship between age and size at maturity differed between males and females and showed that offspring life‐history strategies in O. cincta are primed differently by the parents.     

Mutation risk associated with paternal and maternal age in a cohort of retinoblastoma survivors

Autosomal dominant conditions are known to be associated with advanced paternal age, and it has been suggested that retinoblastoma (Rb) also exhibits a paternal age effect due to the paternal origin of most new germline RB1 mutations. To further our understanding of the association of parental age and risk of de novo germline RB1 mutations, we evaluated the effect of parental age in a cohort of Rb survivors in the United States. A cohort of 262 Rb patients was retrospectively identified at one institution, and telephone interviews were conducted with parents of 160 survivors (65.3%). We classified Rb survivors into three groups: those with unilateral Rb were classified as sporadic if they had no or unknown family history of Rb, those with bilateral Rb were classified as having a de novo germline mutation if they had no or unknown family history of Rb, and those with unilateral or bilateral Rb, who had a family history of Rb, were classified as familial. We built two sets of nested logistic regression models to detect an increased odds of the de novo germline mutation classification related to older parental age compared to sporadic and familial Rb classifications. The modeling strategy evaluated effects of continuous increasing maternal and paternal age and 5-year age increases adjusted for the age of the other parent. Mean maternal ages for survivors classified as having de novo germline mutations and sporadic Rb were similar (28.3 and 28.5, respectively) as were mean paternal ages (31.9 and 31.2, respectively), and all were significantly higher than the weighted general US population means. In contrast, maternal and paternal ages for familial Rb did not differ significantly from the weighted US general population means. Although we noted no significant differences between mean maternal and paternal ages between each of the three Rb classification groups, we found increased odds of a survivor being in the de novo germline mutation group for each 5-year increase in paternal age, but these findings were not statistically significant (de novo vs. sporadic ORs 30-34 = 1.7 [0.7-4], ≥ 35 = 1.3 [0.5-3.3]; de novo vs. familial ORs 30-34 = 2.8 [1.0-8.4], ≥ 35 = 1.6 [0.6-4.6]). Our study suggests a weak paternal age effect for Rb resulting from de novo germline mutations consistent with the paternal origin of most of these mutations.