Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians

The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.

Milking it for all it's worth: The effects of environmental enrichment on maternal nurturance, lactation quality, and offspring social behavior

While alterations in the neonatal environment can have dramatic effects on offspring outcomes, the mechanisms that drive this phenomenon remain unclear. Breastfeeding confers robust benefits to offspring development, including those related to growth, immunity, and neurophysiology. Similarly, improving environmental complexity (i.e., environmental enrichment; EE) contributes developmental advantages to both humans and laboratory animal models. However, the impact of environmental context on maternal care and milk quality has not been thoroughly evaluated, nor are the biological underpinnings of EE on offspring development understood. Here, Sprague-Dawley rats were housed and bred in either EE or standard-housed (SD) conditions. Although EE dams gave birth to a larger number of pups, litters were standardized and cross-fostered across groups on postnatal day (P)1. Maternal milk samples were then collected on P1 (transitional milk phase) and P10 (mature milk phase) for analysis. While EE dams spent less time nursing, postnatal enrichment exposure was associated with heavier offspring bodyweights. Moreover, milk from EE dams had increased triglyceride levels compared to SD dams. Milk from EE mothers also contained a greater microbiome diversity and a significantly higher abundance of bacterial families related to bodyweight and energy metabolism. In addition to changes in lactational quality, we observed sex- and time-dependent effects of EE on offspring social behavior. Specifically, prenatal EE exposure was associated with greater sociability in females, while postnatal EE was associated with greater sociability in male offspring. Together, these results underscore the multidimensional impact of the combined neonatal and maternal environments on offspring development. These data also identify potential deficiencies in the quality of the "gold standard" laboratory housing condition and its impact on the welfare and design of translationally relevant animal models in biomedical research.

Evidence for hybrid breakdown in production of red carotenoids in the marine invertebrate Tigriopus californicus

The marine copepod, Tigriopus californicus, produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This ‘bioconversion’ of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative phosphorylation. Experimental inter-population crosses of lab-reared T. californicus typically produces low-fitness hybrids is due in large part to the disruption of coadapted sets nuclear and mitochondrial genes within the parental populations. These hybrid incompatibilities can increase variability in life history traits and energy production among hybrid lines. Here, we tested if production of astaxanthin was compromised in hybrid copepods and if it was linked to mitochondrial metabolism and offspring development. We observed no clear mitonuclear dysfunction in hybrids fed a limited, carotenoid-deficient diet of nutritional yeast. However, when yellow carotenoids were restored to their diet, hybrid lines produced less astaxanthin than parental lines. We observed that lines fed a yeast diet produced less ATP and had slower offspring development compared to lines fed a more complete diet of algae, suggesting the yeast-only diet may have obscured effects of mitonuclear dysfunction. Astaxanthin production was not significantly associated with development among lines fed a yeast diet but was negatively related to development in early generation hybrids fed an algal diet. In lines fed yeast, astaxanthin was negatively related to ATP synthesis, but in lines fed algae, the relationship was reversed. Although the effects of the yeast diet may have obscured evidence of hybrid dysfunction, these results suggest that astaxanthin bioconversion may still be related to mitochondrial performance and reproductive success.

Maternal postnatal depression and offspring emotional and behavioural development at age 7 years in a UK-birth cohort: the role of paternal involvement

Background: There is considerable variability in emotional and behavioural outcomes of children whose mothers experience depression. Few longitudinal studies have examined potential contributions of dimensions of paternal involvement in the association between maternal postnatal depression (PND) and offspring development. Methods: We examined pathways from maternal PND at 8 weeks postnatally (assessed using the Edinburgh Postnatal Depression Scale) to offspring emotional and behavioural development at 7 years (assessed using the Strengths and Difficulties Questionnaire) through behavioural, affective and cognitive child-focused and mother-influenced dimensions of paternal involvement in 3,434 members of the UK-based birth cohort, the Avon Longitudinal Study of Parents and Children. Analyses were adjusted for a range of baseline confounders and paternal postnatal depression (PND) as an intermediate confounder. Results: Maternal PND was associated with higher levels of some aspects of child-focused and mother-influenced paternal involvement in models accounting for paternal PND, however these pathways were not associated with offspring emotional and behavioural development at age 7 years. There was strong evidence of direct effect from maternal PND to offspring development, but no evidence of mediation through the combination of all indirect pathways through child-focused and mother-influenced paternal involvement. However, higher levels of father-child conflict were associated with increased risk of offspring emotional and behavioural difficulties, and this pathway mediated a proportion of the maternal PND to offspring risk. Additionally, maternal PND was associated with paternal PND, which, in turn, was associated with lower levels of child-focused and mother-influenced paternal involvement. Conclusions: The positive associations between maternal PND and some aspects of paternal involvement suggest that non-depressed fathers may engage in 'compensatory' parenting strategies in response to maternal PND, which although important may not be sufficient in reducing the adverse impact of maternal PND on offspring emotional and behavioural development. Conflictual father-child relationships emerged as a risk factor for adverse offspring development and as an explanatory mechanism in the association between maternal PND and offspring development. These results suggest that interventions that reduce father-child conflict may reduce the risk of emotional and behavioural difficulties in offspring of depressed mothers.

Resistance of Common Bean Genotypes to the Broad Mite, Polyphagotarsonemus latus (Banks, 1904) (Acari: Tarsonemidae): Offspring Development and Biochemical Basis

The broad mite (BM) Polyphagotarsonemus latus is a pest of great prominence for several crops, including the common bean (Phaseolus vulgaris). The objective of this study was to select resistant genotypes and to determine chemicals associated with resistance. In the first experiment, BM incidence was assessed for 36 genotypes in a greenhouse study. A group of 10 genotypes was selected according to the development of BM populations. Mite populations and phytometric and biochemical variables were then determined to study eventual differential genotypic responses to mite infestation. Lower numbers of mite mobile forms (larvae + adults) were found on Verdão, Negrão and Carioca Original genotypes. The magnitude of differences reached 5.4 times more BM in the IAC Alvorada than the Verdão genotype. Plant yields were reduced for the genotypes TAA Bola Cheia, IPR Sabiá, IPR Uirapuru, IAC Alvorada and Carioca Original when plants were infested with BM. The yields for LP 13833, BRS Esteio, Negrão 11, Verdão and MD 1133 were similar between infested and non-infested genotypes, indicating tolerance. Verdão and Negrão 11, besides the tolerance, exhibited low offspring development, indicating antibiosis and/or antixenosis. Higher phenolic compound levels were found in the Verdão genotype. Increased contents of catalase and peroxidase were detected for Negrão 11 genotype when infested with BM. This work allowed the detection of common bean genotypes that express resistance and tolerance to BM. These genotypes can be used in places with a history of BM infestation, or used in breeding programs to incorporate these characteristics in other genotypes.

Cross-seasonal weather effects interact with breeding conditions to impact reproductive success in an alpine songbird

In alpine habitats, fluctuating early-season weather conditions and short breeding seasons limit reproductive opportunities, such that arriving and breeding earlier or later than the optimum may be particularly costly for migratory species. Given early-season energy limitations, the influence of environmental conditions across the annual cycle on breeding phenology may have pronounced fitness consequences, yet our understanding of cross-seasonal dynamics in alpine breeding organisms is severely limited. For an alpine-breeding, migratory population of horned lark (Eremophila alpestris) in northern British Columbia, Canada (54.8N latitude) we assessed how spatially explicit weather conditions from across the annual cycle influenced clutch initiation date and offspring development. We also addressed how cross-seasonal effects on breeding parameters interact to influence reproductive fitness. With 12 years of intensive breeding data and 3 years of migration data from archival light-level geolocators, we used a sliding window approach to identify critical points during the annual cycle where weather events most influenced breeding phenology and offspring development. Consequences for reproductive success were assessed using nest survival simulations. Average clutch initiation varied up to 11 days among years but did not advance from 2003 to 2019. Colder temperatures with greater precipitation at wintering habitats, as well as colder temperatures upon arrival at the breeding site delayed clutch initiation, independent of arrival time. Extreme cold (sub-zero temperatures) within a staging area just prior to arrival at the breeding site carried over to prolong offspring development rate, potentially by influencing parental investment. Nest survival decreased with both later clutch initiation and prolonged offspring development, such that females that nested earlier and fledged offspring at a younger age were up to 45% more likely to reproduce successfully. We demonstrate pronounced carry-over effects acting through mechanisms that influence breeding phenology and offspring development independently. We also highlight the potential importance of staging areas for alpine songbirds, particularly given that environmental conditions are becoming increasingly decoupled across seasons. Understanding the cross-seasonal mechanisms shaping breeding decisions in stochastic environments like the alpine enables more accurate predictions of future individual- and population-level responses to climate change.