RESUMO
Environmental variation often induces plastic responses in organisms that can trigger changes in subsequent generations through non-genetic inheritance mechanisms. Such transgenerational plasticity thus consists of environmentally induced non-random phenotypic modifications that are transmitted through generations. Transgenerational effects may vary according to the sex of the organism experiencing the environmental perturbation, the sex of their descendants or both, but whether they are affected by past sexual selection is unknown. Here, we use experimental evolution on an insect model system to conduct a first test of the involvement of sexual selection history in shaping transgenerational plasticity in the face of rapid environmental change (exposure to pesticide). We manipulated evolutionary history in terms of the intensity of sexual selection for over 80 generations before exposing individuals to the toxicant. We found that sexual selection history constrained adaptation under rapid environmental change. We also detected inter- and transgenerational effects of pesticide exposure in the form of increased fitness and longevity. These cross-generational influences of toxicants were sex dependent (they affected only male descendants), and intergenerational, but not transgenerational, plasticity was modulated by sexual selection history. Our results highlight the complexity of intra-, inter- and transgenerational influences of past selection and environmental stress on phenotypic expression.
Assuntos
Praguicidas , Seleção Sexual , Animais , Masculino , Feminino , Praguicidas/toxicidade , Evolução BiológicaRESUMO
Body size and growth rate can influence individual and population success by mediating fitness. Understanding the factors that influence growth can be difficult to disentangle, however, because growth can be shaped by environmental conditions recently experienced, as well as legacy effects from conditions experienced earlier in life and by parents (via parental effects). To improve understanding of growth among annual cohorts (1982-2015) of Lake Erie Walleye (Sander vitreus), a species with life-history and growth characteristics similar to many other long-lived, iteroparous fishes, we determined the role of the following hypothesised factors: (H1) recent environmental conditions; (H2) traits and experiences of the cohort, including growth, in the previous year; (H3) early-life cohort density; (H4) early-life body size; and (H5) parental composition and environment. We evaluated the relative importance of these hypothesised factors using piecewise structural equation modelling in an information-theoretic framework. Our results indicated that cohort-specific growth of Lake Erie Walleye was most strongly influenced by traits (growth) and experiences of the cohort during the previous year (H2) and parental composition and environment (H5). The observed negative relationship with growth during the previous year may indicate that Walleye exhibit compensatory growth. The relationships with parental sizes and environments may mean that parental contributions to offspring affects cohorts into adulthood, with serious implications for the effects of climate change. Warm winters appear to negatively influence offspring growth performance for many years. Legacy effects had a stronger influence on cohort growth than recent environmental conditions, providing new understanding of how somatic growth is regulated in Lake Erie's Walleye population. Specifically, the parental composition and environment appear important via epigenetic and/or egg-provisioning legacies, with carryover effects modifying growth among years. Ultimately, our findings demonstrate that understanding recent growth in animal populations similar to Lake Erie Walleye may require knowledge of past conditions, including those experienced by parents.
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Parents routinely encounter stress in the ecological environment that can affect offspring development (transgenerational plasticity: TGP); however, parents' interactions with conspecifics may alter how parents respond to ecological stressors. During social buffering, the presence of conspecifics can reduce the response to or increase the speed of recovery from a stressor. This may have cascading effects on offspring if conspecifics can mitigate parental responses to ecological stress in ways that blunt the transmission of stress-induced transgenerational effects. Here, we simultaneously manipulated both paternal social isolation and experience with predation risk prior to fertilisation in threespined stickleback (Gasterosteus aculeatus). We generated offspring via in-vitro fertilisation to allow us to isolate paternal effects mediated via sperm alone (i.e. in the absence of paternal care). If social buffering mitigates TGP induced by paternal exposure to predation risk, then we expect the transgenerational effects of predation exposure to be weaker when a conspecific is present compared to when the father is isolated. Offspring of predator-exposed fathers showed reduced anxiety-like behaviour and tended to be captured faster by the predator. Fathers who were socially isolated also had offspring that were captured faster by a live predator, suggesting that paternal social isolation may have maladaptive effects on how offspring respond to ecological stressors. Despite additive effects of paternal social isolation and paternal predation risk, we found no evidence of an interaction between these paternal treatments, suggesting that the presence of a conspecific did not buffer fathers and/or offspring from the effects of predation risk. Our results suggest that socially induced stress is an important, yet underappreciated, mediator of TGP and can elicit transgenerational effects even in species that do not form permanent social groups. Future studies should therefore consider how the parental social environment can affect both within and trans-generational responses to ecological stressors.
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I document the transmission of a grandfather's net nutritional deprivation and psychosocial stress in young adulthood across multiple generations using the grandfather's ex-prisoner of war (ex-POW) status in the U.S. Civil War (1861-1865). Using a newly created dataset, I uncover an association between a grandfather's ex-POW status and the longevity after age 45 of his sons and male-line grandsons but not of his daughters, granddaughters, female-line grandsons, children-in-law, or grandchildren-in-law. Male-line grandsons lost roughly a year of life at age 45 (4% of remaining life expectancy) if descended from ex-POWs who suffered severe captivity conditions than if descended from non-POWs. If their grandfathers faced a less harsh captivity, male-line grandsons lost less than a year of life compared with those descended from non-POWs. I find that the grandfather's age at exposure and the grandson's education, as well as the son's and the grandson's poor late gestational conditions (proxied by season of birth), mediate this relationship. I rule out socioeconomic status, marriage and mortality selection, and cultural or psychological transmission from grandfathers to grandsons as explanations. I cannot rule out an epigenetic explanation.
Assuntos
Avós , Prisioneiros , Transtornos de Estresse Pós-Traumáticos , Criança , Humanos , Masculino , Feminino , Gravidez , Adulto Jovem , Adulto , Pessoa de Meia-Idade , Longevidade , Família/psicologia , Casamento/psicologia , Transtornos de Estresse Pós-Traumáticos/psicologiaRESUMO
The environment plays an important role in an individual's development during early life, however, parents may also influence offspring development through so called "parental effects." We examined the effects of environmental enrichment in zebrafish (Danio rerio) across two generations through the paternal lineage. Fathers and grandfathers were exposed to either standard or high levels of housing enrichment for 4-weeks during adulthood. First-generation (F1) and second-generation (F2) offspring were obtained from controlled breeding and tested as larvae for changes in morphology at hatching stage (72hpf), and in locomotor activity at larval stage (120hpf) in both generations. We found paternal experience of enrichment resulted in changes in trunk length of F1 offspring and changes in spine curvature and dorsal length of F2 offspring, while changes in snout morphology of F2 offspring seemed to be driven by whether grandpaternal and paternal experience of the environment was matched or not. We found that while paternal enrichment increased the frequency of spontaneous movement in F1 and F2 offspring, interacting effects of paternal and grandpaternal enrichment on movement distance were seen in F2 offspring, and that spontaneous movement and the distance that larvae swam are thus distinct phenotypes that were differentially affected by the experiences of previous paternal generations. Taken together, these findings suggest that the parental and grandparental environment influence zebrafish behavior and morphology. The nature of these effects and the design of this study mean that these phenotypes were likely the result of nongenetic transmission through the paternal germline.
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Células Germinativas , Peixe-Zebra , Animais , Peixe-Zebra/genética , FenótipoRESUMO
The global consumption of highly processed, calorie-dense foods has contributed to an epidemic of overweight and obesity, along with negative consequences for metabolic dysfunction and disease susceptibility. As it becomes apparent that overweight and obesity have ripple effects through generations, understanding of the processes involved is required, in both maternal and paternal epigenetic inheritance. We focused on the patrilineal effects of a Western-style high-fat (21%) and high-sugar (34%) diet (WD) compared to control diet (CD) during adolescence and investigated F0 and F1 mice for physiological and behavioral changes. F0 males (fathers) showed increased body weight, impaired glycemic control, and decreased attractiveness to females. Paternal WD caused significant phenotypic changes in F1 offspring, including higher body weights of pups, increased Actinobacteria abundance in the gut microbiota (ascertained using 16S microbiome profiling), a food preference for WD pellets, increased male dominance and attractiveness to females, as well as decreased behavioral despair. These results collectively demonstrate the long-term intergenerational effects of a Western-style diet during paternal adolescence. The behavioral and physiological alterations in F1 offspring provide evidence of adaptive paternal programming via epigenetic inheritance. These findings have important implications for understanding paternally mediated intergenerational inheritance, and its relevance to offspring health and disease susceptibility.
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Comportamento Animal , Dieta Ocidental , Microbioma Gastrointestinal , Herança Paterna , Comportamento Social , Estresse Fisiológico , Animais , Feminino , Masculino , CamundongosRESUMO
Paternal stress exposure is known to impact the development of stress-related behaviors in offspring. Previous work has highlighted the importance of sperm mediated factors, such as RNAs, in transmitting the effects of parental stress. However, a key unanswered question is whether mothers behavior could drive or modulate the transmission of paternal stress effects on offspring development. Here we investigate how chronic variable stress in Balb/C mice influences the sex-specific development of anxiety- and depression-like neural and behavioral development in offspring. Moreover, we examined how stressed fathers influenced mate maternal investment towards their offspring and how this may modulate the transmission of paternal stress effects on offspring. We show that paternal stress leads to sex-specific effects on offspring behavior. Males that are chronically stressed sire female offspring that show increased anxiety and depression-like behaviors. However, male offspring of stressed fathers show reductions in anxiety- and depression-behaviors and are generally more exploratory. Moreover, we show that females mated with stressed males gain less weight during pregnancy and provide less care towards their offspring which additionally influenced offspring development. These data indicate that paternal stress can influence offspring development both directly and indirectly via changes in mothers, with implications for sex-specific offspring development.
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Mães , Sêmen , Gravidez , Camundongos , Animais , Humanos , Masculino , Feminino , Pai , Reprodução , Comportamento Materno , Exposição PaternaRESUMO
There is growing evidence that offspring receive information about their environment vertically, i.e. from their parents (environmental parental effects or transgenerational plasticity). For example, parents exposed to predation risk may produce offspring with heightened antipredator defences. At the same time, organisms can gain information about the environment horizontally, from conspecifics. In this study, we provide some of the first evidence that horizontally acquired social information can be transmitted vertically across generations. Three-spined stickleback (Gasterosteus aculeatus) fathers produced larval offspring with altered antipredator behaviour when fathers received visual and olfactory cues from predator-chased neighbours. Although fathers did not personally witness their neighbours being chased (i.e. they never saw the predator), changes in offspring traits were similar to those induced by direct paternal exposure to predation risk. These findings suggest that two different non-genetic pathways (horizontal transfer of social information, vertical transfer via sperm-mediated paternal effects) can combine to affect offspring phenotypes. The implications of simultaneous horizontal and vertical transmission are widely appreciated in the context of disease and culture; our results suggest that they could be equally important for the maintenance of phenotypic variation and could have profound consequences for the rate at which information flows within and across generations.
Assuntos
Smegmamorpha , Animais , Masculino , Herança Paterna , Fenótipo , Comportamento Predatório , Sêmen , Smegmamorpha/genéticaRESUMO
Intergenerational effects from fathers to offspring are increasingly reported from diverse organisms, but the underlying mechanisms remain speculative. Paternal trans-generational immune priming (TGIP) was demonstrated in the red flour beetle Tribolium castaneum: non-infectious bacterial exposure of fathers protects their offspring against an infectious challenge for at least two generations. Epigenetic processes, such as cytosine methylation of nucleic acids, have been proposed to enable transfer of information from fathers to offspring. Here we studied a potential role in TGIP of the Dnmt2 gene (renamed as Trdmt1 in humans), which encodes a highly conserved enzyme that methylates different RNAs, including specific cytosines of a set of tRNAs. Dnmt2 has previously been reported to be involved in intergenerational epigenetic inheritance in mice and protection against viruses in fruit flies. We first studied gene expression and found that Dnmt2 is expressed in various life history stages and tissues of T. castaneum, with high expression in the reproductive organs. RNAi-mediated knockdown of Dnmt2 in fathers was systemic, slowed down offspring larval development and increased mortality of the adult offspring upon bacterial infection. However, these effects were independent of bacterial exposure of the fathers. In conclusion, our results point towards a role of Dnmt2 for paternal effects, while elucidation of the mechanisms behind paternal TGIP needs further studies.
Assuntos
Besouros , DNA (Citosina-5-)-Metiltransferases , Proteínas de Insetos , Animais , Masculino , Besouros/genética , Citosina , DNA (Citosina-5-)-Metiltransferases/genética , RNA de Transferência , Técnicas de Silenciamento de Genes , Proteínas de Insetos/genética , Suscetibilidade a DoençasRESUMO
The evidence supports the occurrence of environmentally-induced paternal epigenetic inheritance that shapes the offspring phenotype in the absence of direct or indirect paternal care and clearly demonstrates that sperm epigenetics is one of the major actors mediating these paternal effects. However, in most animals, while sperm makes up only a small portion of the seminal fluid, males also have a complex mixture of proteins, peptides, different types of small noncoding RNAs, and cell-free DNA fragments in their ejaculate. These seminal fluid contents (Sfcs) are in close contact with the reproductive cells, tissues, organs, and other molecules of both males and females during reproduction. Moreover, their production and use are adjusted in response to environmental conditions, making them potential markers of environmentally- and developmentally-induced paternal effects on the next generation(s). Although there is some intriguing evidence for Sfc-mediated paternal effects, the underlying molecular mechanisms remain poorly defined. In this review, the current evidence regarding the links between seminal fluid and environmental paternal effects and the potential pathways and mechanisms that seminal fluid may follow in mediating paternal epigenetic inheritance are discussed.
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Ácidos Nucleicos , Herança Paterna , Animais , Feminino , Masculino , Sêmen , Ácidos Nucleicos/metabolismo , Espermatozoides/metabolismo , Epigênese GenéticaRESUMO
Parental effects can prepare offspring for different environments and facilitate survival across generations. We exposed parental populations of the estuarine anemone, Nematostella vectensis, from Massachusetts to elevated temperatures and quantified larval mortality across a temperature gradient. We found that parental exposure to elevated temperatures resulted in a consistent increase in larval thermal tolerance, as measured by the temperature at which 50% of larvae die (LT50), with a mean increase in LT50 of 0.3°C. Larvae from subsequent spawns returned to baseline thermal thresholds when parents were returned to normal temperatures, indicating plasticity in these parental effects. Histological analyses of gametogenesis in females suggested that these dynamic shifts in larval thermal tolerance may be facilitated by maternal effects in non-overlapping gametic cohorts. We also compared larvae from North Carolina (a genetically distinct population with higher baseline thermal tolerance) and Massachusetts parents, and observed that larvae from heat-exposed Massachusetts parents had thermal thresholds comparable to those of larvae from unexposed North Carolina parents. North Carolina parents also increased larval thermal tolerance under the same high-temperature regime, suggesting that plasticity in parental effects is an inherent trait for N. vectensis Overall, we find that larval thermal tolerance in N. vectensis shows a strong genetic basis and can be modulated by parental effects. Further understanding of the mechanisms behind these shifts can elucidate the fate of thermally sensitive ectotherms in a rapidly changing thermal environment.
Assuntos
Anemone , Animais , Feminino , Temperatura Alta , Larva , Massachusetts , North CarolinaRESUMO
There has been an explosion of recent evidence that environments experienced by fathers or their ejaculates can influence offspring phenotypes (paternal effects). However, little is known about whether such effects are adaptive, which would have far-reaching implications for the many species facing rapidly changing environments. For example, some arguments suggest paternal effects might be a source of cross-generational plasticity, preparing offspring to face similar conditions to their father (anticipatory hypothesis). Alternatively, ejaculate-mediated effects on offspring may be non-adaptive by-products of stress. Here, we conduct an experiment to distinguish between these predictions, exposing ejaculates of the externally fertilizing mussel Mytilus galloprovincialis to ambient (19°C) and high (24°C) temperatures, then rearing offspring groups in temperatures that match and mismatch those of sperm. We find that, overall, high temperature-treated sperm induced higher rates of normal offspring development and higher success in transitioning to second-stage larvae, which may represent adaptive epigenetic changes or selection on sperm haplotypes. However, the progeny of high temperature-treated sperm did not perform better than those of ambient temperature-treated sperm when rearing temperatures were high. Overall, these findings offer little support for the anticipatory hypothesis and suggest instead that beneficial paternal effects may be eroded when offspring develop under stressful conditions.
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Mytilus edulis , Herança Paterna , Animais , Fertilização , Masculino , Fenótipo , EspermatozoidesRESUMO
A recent meta-analysis concluded, 'transgenerational effects are widespread, strong and persistent'. We identify biases in the literature search, data and analyses, questioning that conclusion. Re-analyses indicate few studies actually tested transgenerational effects - making it challenging to disentangle condition-transfer from anticipatory parental effects, and providing little insight into the underlying mechanisms.
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AbstractOxidative stress (OS) experienced early in life can affect an individual's phenotype. However, its consequences for the next generation remain largely unexplored. We manipulated the OS level endured by zebra finches (Taeniopygia guttata) during their development by transitorily inhibiting the synthesis of the key antioxidant glutathione ("early-high-OS"). The offspring of these birds and control parents were cross fostered at hatching to enlarge or reduce its brood size. Independent of parents' early-life OS levels, the chicks raised in enlarged broods showed lower erythrocyte glutathione levels, revealing glutathione sensitivity to environmental conditions. Control biological mothers produced females, not males, that attained a higher body mass when raised in a benign environment (i.e., the reduced brood). In contrast, biological mothers exposed to early-life OS produced heavier males, not females, when allocated in reduced broods. Early-life OS also affected the parental rearing capacity because 12-day-old nestlings raised by a foster pair with both early-high-OS members grew shorter legs (tarsus) than chicks from other groups. The results indicate that environmental conditions during development can affect early glutathione levels, which may in turn influence the next generation through both pre- and postnatal parental effects. The results also demonstrate that early-life OS can constrain the offspring phenotype.
Assuntos
Antioxidantes/metabolismo , Tentilhões/crescimento & desenvolvimento , Glutationa/metabolismo , Estresse Oxidativo/fisiologia , Animais , Tornozelo/crescimento & desenvolvimento , Peso Corporal , Butionina Sulfoximina/farmacologia , Tamanho da Ninhada , Eritrócitos/química , Feminino , Tentilhões/metabolismo , Glutationa/efeitos dos fármacos , Masculino , Comportamento de Nidação/fisiologiaRESUMO
The mammalian placenta is both the physical interface between mother and fetus, and the source of endocrine signals that target the maternal hypothalamus, priming females for parturition, lactation and motherhood. Despite the importance of this connection, the effects of altered placental signalling on the maternal brain are insufficiently studied. Here, we show that placental dysfunction alters gene expression in the maternal brain, with the potential to affect maternal behaviour. Using a cross between the house mouse and the Algerian mouse, in which hybrid placental development is abnormal, we sequenced late-gestation placental and maternal medial preoptic area transcriptomes and quantified differential expression and placenta-maternal brain co-expression between normal and hybrid pregnancies. The expression of Fmn1 and Drd3 was significantly altered in the brains of females exposed to hybrid placentas. Most strikingly, expression patterns of placenta-specific gene families and Drd3 in the brains of house mouse females carrying hybrid litters matched those of female Algerian mice, the paternal species in the cross. Our results indicate that the paternally derived placental genome can influence the expression of maternal-fetal communication genes, including placental hormones, suggesting an effect of the offspring's father on the mother's brain.
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Encéfalo/fisiologia , Expressão Gênica/fisiologia , Comportamento Materno , Placenta/fisiologia , Animais , Quimera , Feminino , Camundongos , GravidezRESUMO
Sperm cells experience considerable post-ejaculation environmental variation. However, little is known about whether this affects their molecular composition, probably owing to the assumption that sperm are transcriptionally quiescent. Nevertheless, recent evidence shows sperm have distinct RNA profiles that affect fertilization and embryo viability. Moreover, RNAs are expected to be highly sensitive to extracellular changes. One such group of RNAs are heat shock protein (hsp) transcripts, which function in stress responses and are enriched in sperm. Here, we exploit the experimental tractability of the mussel Mytilus galloprovincialis by exposing paired samples of ejaculated sperm to ambient (19°C) and increased (25°C) temperatures, then measure (i) sperm motility phenotypes, and (ii) messenger RNA (mRNA) levels of two target genes (hsp70 and hsp90) and several putative reference genes. We find no phenotypic changes in motility, but reduced mRNA levels for hsp90 and the putative reference gene gapdh at 25°C. This could reflect either decay of specific RNAs, or changes in translation and degradation rates of transcripts to maintain sperm function under stress. These findings represent, to our knowledge, the first evidence for changes in sperm RNA profiles owing to post-ejaculation environments, and suggest that sperm may be more vulnerable to stress from rising temperatures than currently thought.
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Ejaculação/fisiologia , Mytilus/fisiologia , RNA , Espermatozoides/fisiologia , Animais , Proteínas de Choque Térmico HSP70/genética , Proteínas de Choque Térmico HSP90/genética , Proteínas de Choque Térmico/metabolismo , Resposta ao Choque Térmico/fisiologia , Humanos , Masculino , RNA Mensageiro/metabolismo , Motilidade dos Espermatozoides , TemperaturaRESUMO
The Kinship Theory of Genomic Imprinting (KTGI) posits that, in species where females mate with multiple males, there is selection for a male to enhance the reproductive success of his offspring at the expense of other males and his mating partner. Reciprocal crosses between honey bee subspecies show parent-of-origin effects for reproductive traits, suggesting that males modify the expression of genes related to female function in their female offspring. This effect is likely to be greater in the Cape honey bee (Apis mellifera capensis), because a male's daughters have the unique ability to produce female offspring that can develop into reproductive workers or the next queen without mating. We generated reciprocal crosses between Capensis and another subspecies and used RNA-seq to identify transcripts that are over- or underexpressed in the embryos, depending on the parental origin of the gene. As predicted, 21 genes showed expression bias towards the Capensis father's allele in colonies with a Capensis father, with no such bias in the reciprocal cross. A further six genes showed a consistent bias towards expression of the father's allele across all eight colonies examined, regardless of the direction of the cross. Consistent with predictions of the KTGI, six of the 21 genes are associated with female reproduction. No gene consistently showed overexpression of the maternal allele.
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Impressão Genômica , Reprodução , Alelos , Animais , Abelhas/genética , Feminino , Expressão Gênica , Masculino , FenótipoRESUMO
While the importance of maternal effects has long been appreciated, a growing body of evidence now points to the paternal environment having an important influence on offspring phenotype. Indeed, research on rodent models suggests that paternal stress leaves an imprint on the behaviour and physiology of offspring via nongenetic information carried in the spermatozoa; however, fish have been understudied with regard to these sperm-mediated effects. Here, we investigated whether the zebrafish was subjected to heritable influences of paternal stress by exposing males to stressors (conspecific-derived alarm cue, chasing and bright light) before mating and assessing the behavioural and endocrine responses of their offspring, including their behavioural response to conspecific-derived alarm cue. We found that after males are exposed to stress, their larval offspring show weakened responses to stressors. Small RNA sequencing subsequently revealed that the levels of several small noncoding RNAs, including microRNAs, PIWI-interacting RNAs and tRNA-derived small RNAs, were altered in the spermatozoa of stressed fathers, suggesting that stress-induced alterations to the spermatozoal RNA landscape may contribute to shaping offspring phenotype. The work demonstrates that paternal stress should not be overlooked as a source of phenotypic variation and that spermatozoal small RNAs may be important intergenerational messengers in fish.
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MicroRNAs , Herança Paterna , Pequeno RNA não Traduzido , Espermatozoides , Peixe-Zebra/genética , Animais , Epigênese Genética , Masculino , MicroRNAs/genética , Pequeno RNA não Traduzido/genética , Estresse FisiológicoRESUMO
There is increasing interest within the genetics community in estimating the relative contribution of parental genetic effects on offspring phenotypes. Here we describe the user-friendly M-GCTA software package used to estimate the proportion of phenotypic variance explained by maternal (or alternatively paternal) and offspring genotypes on offspring phenotypes. The tool requires large studies where genome-wide genotype data are available on mother- (or alternatively father-) offspring pairs. The software includes several options for data cleaning and quality control, including the ability to detect and automatically remove cryptically related pairs of individuals. It also allows users to construct genetic relationship matrices indexing genetic similarity across the genome between parents and offspring, enabling the estimation of variance explained by maternal (or alternatively paternal) and offspring genetic effects. We evaluated the performance of the software using a range of data simulations and estimated the computing time and memory requirements. We demonstrate the use of M-GCTA on previously analyzed birth weight data from two large population based birth cohorts, the Avon Longitudinal Study of Parents and Children (ALSPAC) and the Norwegian Mother and Child Cohort Study (MoBa). We show how genetic variation in birth weight is predominantly explained by fetal genetic rather than maternal genetic sources of variation.
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Peso ao Nascer/genética , Previsões/métodos , Criança , Estudos de Coortes , Simulação por Computador , Pai , Feminino , Estudo de Associação Genômica Ampla/métodos , Genótipo , Humanos , Estudos Longitudinais , Masculino , Herança Materna/fisiologia , Modelos Genéticos , Mães , Pais , Herança Paterna/fisiologia , Fenótipo , SoftwareRESUMO
Sex role reversal is not uncommon in the animal kingdom but is taken to the extreme by the Syngnathidae, in which male pregnancy is one of the most astonishing idiosyncrasies. However, critical and time-dependent environmental effects on developing embryos, such as those extensively studied in mammalian pregnancy, have not been investigated in the male pregnancy context. Here, we tested the hypothesis that seahorse pregnancy is subject to 'critical windows' of environmental sensitivity by feeding male long-snouted seahorses (Hippocampus reidi) a diet deficient in polyunsaturated fatty acids during specific periods before and during pregnancy. Despite embryos being nourished principally by maternally supplied yolk, we found that offspring morphology, fatty acid composition and gene expression profiles were influenced by paternal diet in a manner that depended critically on the timing of manipulation. Specifically, reception of a diet deficient in polyunsaturated fatty acids in the days preceding pregnancy resulted in smaller newborn offspring, while the same diet administered towards the end of pregnancy resulted in substantial alterations to newborn gene expression and elongation of the snout at 10 days old. Although paternal diet did not affect 10 day survival, the observed morphological alterations in some cases could have important fitness consequences in the face of natural selective pressures such as predation and food availability. Our results demonstrate that, under male pregnancy, fine-scale temporal variation in parental diet quality and subsequent critical window effects should not be overlooked as determinants of developing offspring fitness.