Reply to Technical Comment on Jonason, P. K., & Luoto, S. (2021). The dark side of the rainbow: Homosexuals and bisexuals have higher Dark Triad traits than heterosexuals. Personality and Individual Differences, 181, 111040.

We thank Sharpe and colleagues for the opportunity to discuss our article titled “The dark side of the rainbow: Homosexuals and bisexuals have higher Dark Triad traits than heterosexuals” in more detail. Here, we address the methodological concerns raised by Sharpe et al. and conclude by discussing our critics’ problematic suggestion that there is something pathologically “wrong” with homosexual and bisexual people. As scientists, we avoid moralizing on such topics, instead openly reporting the results of our research, even hypothesizing that elevated Dark Triad traits in nonheterosexual individuals might constitute an adaptive response or a predictive adaptive response to environmental harshness, whether such harshness may be experienced prenatally, in adolescence, or in adulthood. We further wish to reject and distance ourselves from the prejudiced view of homosexuality voiced by Sharpe et al. Their suggestion to avoid the term “homosexuality” is in itself prejudiced and in stark opposition to the liberation and empowerment of people with same-sex sexual attractions. We encourage other sex researchers to continue using the term “homosexual” as a purely descriptive scientific term which carries no moral implications, and the relevant communities and organizations to accept its continued use in science alongside other sexual orientation categories.

Rhesus macaques compensate for reproductive delay following ecological adversity early in life

Adversity early in life can shape the reproductive potential of individuals through negative effects on health and lifespan. However, long-lived populations with multiple reproductive events may present alternative life history strategies to optimize reproductive schedules and compensate for shorter lifespans when experiencing adversities early in life. Here, we quantify the effects of major hurricanes and density-dependence as sources of early-life ecological adversity on the mean age-specific fertility, reproductive pace, and lifetime reproductive success (LRS) of Cayo Santiago rhesus macaque females, and explored demographic mechanisms for reproductive schedule optimization later in life. Females experiencing major hurricanes early in life exhibit a delayed reproductive debut, but maintain inter-birth intervals and show a higher mean fertility during prime reproductive ages relative to females experiencing no hurricanes. Increasing density at birth is associated to a decrease in mean fertility and LRS. When combined, our study reveals that early-life ecological adversities predict a delay-overshoot pattern in mean age-specific fertility that supports the maintenance of LRS. In contrast to predictive adaptive response models of accelerated reproduction, the long-lived Cayo Santiago population presents a novel reproductive strategy where females who experience major natural disasters early in life ultimately overcome their initial reproductive penalty with no overall negative fitness outcomes. Such strategy suggests that investing more energy into development and maintenance at younger ages allows long-lived females experiencing early-life ecological adversity to reproduce at a mean rate equivalent to that of a typical female cohort later in life.

A model of optimal timing for a predictive adaptive response

Predictive adaptive responses (PARs) are a form of developmental plasticity in which the developmental response to an environmental cue experienced early in life is delayed and yet, at the same time, the induced phenotype anticipates (i.e., is completely developed before) exposure to the eventual environmental state predicted by the cue, in which the phenotype is adaptive. We model this sequence of events to discover, under various assumptions concerning the cost of development, what lengths of delay, developmental time, and anticipation are optimal. We find that in many scenarios modeled, development of the induced phenotype should be completed at the exact same time that the environmental exposure relevant to the induced phenotype begins: that is, in contrast to our observed cases of PARs, there should be no anticipation. Moreover, unless slow development is costly, development should commence immediately after the cue: there should be no delay. Thus, PARs, which normally have non-zero delays and/or anticipation, are highly unusual. Importantly, the exceptions to these predictions of zero delays and anticipation occurred when developmental time was fixed and delaying development was increasingly costly. We suggest, therefore, that PARs will only evolve under three kinds of circumstances: (i) there are strong timing constraints on the cue and the environmental status, (ii) delaying development is costly, and development time is either fixed or slow development is costly, or (iii) when the period between the cue and the eventual environmental change is variable and the cost of not completing development before the change is high. These predictions are empirically testable.

Mismatched Prenatal and Postnatal Maternal Depressive Symptoms and Child Behaviours: A Sex-Dependent Role for NR3C1 DNA Methylation in the Wirral Child Health and Development Study

Evolutionary hypotheses predict that male fetuses are more vulnerable to poor maternal conditions (Sex-biased Maternal Investment), but female fetuses are at greater risk of glucocorticoid-mediated disorders where there is a mismatch between fetal and postnatal environments (Predictive Adaptive Response). Self-reported prenatal and postnatal depression and maternal report of child anxious-depressed symptoms at 2.5, 3.5 and 5.0 years were obtained from an ‘extensive’ sample of first-time mothers (N = 794). Salivary NR3C1 1-F promoter methylation was assayed at 14 months in an ‘intensive’ subsample (n = 176) and stratified by psychosocial risk. Generalised structural equation models were fitted and estimated by maximum likelihood to allow the inclusion of participants from both intensive and extensive samples. Postnatal depression was associated with NR3C1 methylation and anxious-depressed symptoms in daughters of mothers with low prenatal depression (prenatal-postnatal depression interaction for methylation, p < 0.001; for child symptoms, p = 0.011). In girls, NR3C1 methylation mediated the association between maternal depression and child anxious-depressed symptoms. The effects were greater in girls than boys: the test of sex differences in the effect of the prenatal-postnatal depression interaction on both outcomes gave X2 (2) = 5.95 (p = 0.051). This was the first human study to show that epigenetic and early behavioural outcomes may arise through different mechanisms in males and females.

Preterm birth in evolutionary context: a predictive adaptive response?

Preterm birth is a significant public health problem worldwide, leading to substantial mortality in the newborn period, and a considerable burden of complications longer term, for affected infants and their carers. The fact that it is so common, and rates vary between different populations, raising the question of whether in some circumstances it might be an adaptive trait. In this review, we outline some of the evolutionary explanations put forward for preterm birth. We specifically address the hypothesis of the predictive adaptive response, setting it in the context of the Developmental Origins of Health and Disease, and explore the predictions that this hypothesis makes for the potential causes and consequences of preterm birth. We describe how preterm birth can be triggered by a range of adverse environmental factors, including nutrition, stress and relative socioeconomic status. Examining the literature for any associated longer-term phenotypic changes, we find no strong evidence for a marked temporal shift in the reproductive life-history trajectory, but more persuasive evidence for a re-programming of the cardiovascular and endocrine system, and a range of effects on neurodevelopment. Distinguishing between preterm birth as a predictive, rather than immediate adaptive response will depend on the demonstration of a positive effect of these alterations in developmental trajectories on reproductive fitness. This article is part of the theme issue ‘Developing differences: early-life effects and evolutionary medicine'.

Intergenerational response of steroidogenesis-related genes to maternal malnutrition

We sought to examine whether rat maternal food restriction (MFR) affects the expression of steroidogenesis-related genes Cyp19, Cyp17a1, Insl3 and Gdf-9 in the ovaries of offspring from the first (FRG1) and second (FRG2) generations at pre-pubertal age (week 4) and during adulthood (week 8). At week 4, MFR significantly increased the expression of RNAs for all analyzed genes in both FRG1 and FRG2 females, which may indicate that MFR affects the onset of the reproductive lifespan, by inducing early pubertal onset. At week 8, the Cyp19 gene was still upregulated in MRF-subjected animals (Cyp19: P=0.0049 and P=0.0508 in FRG1 and FRG2, respectively), but MFR induced a significant decrease in Cyp17 and Gdf-9 gene expression in the offspring of both FRG1 and FRG2 females when compared with the controls (Cyp17: P=0.0018 and P=0.0016, respectively; Gdf-9: P=0.0047 and P=0.0023, respectively). This suggests that females at week 8, which should normally be in their optimal reproductive capacity, experience premature ovarian aging. At week 4, the activation of Cyp19 and Cyp17 was higher in the FRG1 ovaries than in the FRG2 ovaries, whereas the extent of Insl3 and Gdf-9 activation was lower in the FRG1 ovaries. This may indicate that FRG2 females were more vulnerable to MFR than their mothers (FRG1) and grandmothers, which is consistent with the ‘predictive adaptive response’ hypothesis. Our findings reveal that MFR may induce intergenerational ovarian changes as an adaptive response to ensure reproductive success before death.

A ‘phenotypic hangover’ – the predictive adaptive response and multigenerational effects of altered nutrition on the transcriptome of Drosophila melanogaster

The Developmental Origins of Health and Disease (DOHaD) hypothesis predicts that early-life environmental exposures can be detrimental to later-life health, and that mismatch between the pre- and postnatal environment may contribute to the growing non-communicable disease (NCD) epidemic. Within this is an increasingly recognised role for epigenetic mechanisms; epigenetic modifications can be influenced by, e.g., nutrition, and can alter gene expression in mothers and offspring. Currently, there are no whole-genome transcriptional studies of response to nutritional alteration. Thus, we sought to explore how nutrition affects the expression of genes involved in epigenetic processes in Drosophila melanogaster. We manipulated Drosophila food macronutrient composition at the F0 generation, mismatched F1 offspring back to a standard diet, and analysed the transcriptome of the F0 – F3 generations by RNA-sequencing. At F0, the altered (high protein, low carbohydrate, HPLC) diet increased expression of genes involved in epigenetic processes, with coordinated downregulation of genes involved in immunity, neurotransmission and neurodevelopment, oxidative stress and metabolism. Upon reversion to standard nutrition, mismatched F1 and F2 generations displayed multigenerational inheritance of altered gene expression. By the F3 generation, gene expression had reverted to F0 (matched) levels. These nutritionally-induced gene expression changes demonstrate that dietary alteration can upregulate epigenetic genes, which may influence the expression of genes with broad biological functions. Further, the multigenerational inheritance of the gene expression changes in F1 and F2 mismatched generations suggests a predictive adaptive response (PAR) to maternal nutrition. Our findings may help to understand the interaction between maternal diet and future offspring health, and have direct implications for the current NCD epidemic.

Long-term fitness consequences of early environment in a long-lived ungulate

Cohort effects can be a major source of heterogeneity and play an important role in population dynamics. Silver-spoon effects, when environmental quality at birth improves future performance regardless of the adult environment, can induce strong lagged responses on population growth. Alternatively, the external predictive adaptive response (PAR) hypothesis predicts that organisms will adjust their developmental trajectory and physiology during early life in anticipation of expected adult conditions but has rarely been assessed in wild species. We used over 40 years of detailed individual monitoring of bighorn ewes ( Ovis canadensis ) to quantify long-term cohort effects on survival and reproduction. We then tested both the silver-spoon and the PAR hypotheses. Cohort effects involved a strong interaction between birth and current environments: reproduction and survival were lowest for ewes that were born and lived at high population densities. This interaction, however, does not support the PAR hypothesis because individuals with matching high-density birth and adult environments had reduced fitness. Instead, individuals born at high density had overall lower lifetime fitness suggesting a silver-spoon effect. Early-life conditions can induce long-term changes in fitness components, and their effects on cohort fitness vary according to adult environment.