A trade-off between reproductive investment and maternal cerebellum size in a precocial bird

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this record.Natural selection favours increased investment in reproduction, yet considerable variation in parental investment is observed in natural populations. Life-history theory predicts that this variation is maintained by a trade-off between the benefits of increased reproductive investment and its associated costs for the parents. The nature of these costs of reproduction, however, remains poorly understood. The brain is an energetically highly expensive organ and increased reproductive investment may, therefore, negatively affect brain maintenance. Using artificial selection lines for high and low prenatal maternal investment in a precocial bird, the Japanese quail (Coturnix japonica), we provide experimental evidence for this hypothesis by showing that increased prenatal provisioning negatively affects the size of a particular brain region of the mother, the cerebellum. Our finding suggests that cognitive demands may constrain the evolution of parental investment, and vice versa, contributing to the maintenance of variation in reproductive behaviour in animal populations.This work was supported by the Swiss National Science Foundation (PP00P3_128386, PP00P3_157455 to B.T.) and the Georges und Antoine Claraz-Schenkung (to C.E.)

Long-term effect of yolk carotenoid levels on testis size in a precocial bird

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this record.Conditions experienced during prenatal development can have long-lasting organizational effects on offspring. Maternal carotenoids deposited in the eggs of birds and other oviparous species play an important role during fast embryonic growth and chick development through their antioxidant properties. However, the long-term consequences of variation in maternal carotenoid transfer for the offspring have seldom been considered. Since plasma carotenoid levels at adulthood are known to influence testis size and yolk carotenoid levels influence the ability to extract carotenoids later in life, we hypothesized that maternally transmitted carotenoids might influence gonad size at adulthood. Here, we showed that male Japanese quail (Coturnix japonica) originating from a carotenoid-enriched egg had smaller testes than control individuals at adulthood. This result shows that yolk carotenoids have long-term organizational effects. In addition, given that carotenoid intake at sexual maturity increases sperm quality and that a decreased testis size is associated with a lower sperm production, we propose that carotenoid exposure during embryo development might influence a trade-off between ejaculate size and sperm quality.The study was supported by the Swiss National Science Foundation (PP00P3_128386 and PP00P3_157455) and the Fonds zur Förderung des akademischen Nachwuchses

Disentangling Genetic and Prenatal Maternal Effects on Offspring Size and Survival

This is the author accepted manuscript. The final version is available from University of Chicago Press via the DOI in this record.Organizational processes during prenatal development can have long-term effects on an individual's phenotype. Because these early developmental stages are sensitive to environmental influences, mothers are in a unique position to alter their offspring's phenotype by differentially allocating resources to their developing young. However, such prenatal maternal effects are difficult to disentangle from other forms of parental care, additive genetic effects, and/or other forms of maternal inheritance, hampering our understanding of their evolutionary consequences. Here we used divergent selection lines for high and low prenatal maternal investment and their reciprocal line crosses in a precocial bird-the Japanese quail (Coturnix japonica)-to quantify the relative importance of genes and prenatal maternal effects in shaping offspring phenotype. Maternal but not paternal origin strongly affected offspring body size and survival throughout development. Although the effects of maternal egg investment faded over time, they were large at key life stages. Additionally, there was evidence for other forms of maternal inheritance affecting offspring phenotype at later stages of development. Our study is among the first to successfully disentangle prenatal maternal effects from all other sources of confounding variation and highlights the important role of prenatal maternal provisioning in shaping offspring traits closely linked to fitness.The study was financially supported by the Swiss National Science Foundation (PP00P3_128386 and PP00P3_157455 to B.T.)

Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this record.Maternal effects can adaptively modulate offspring developmental trajectories in variable but predictable environments. Hormone synthesis is sensitive to environmental factors, and maternal hormones are thus a powerful mechanism to transfer environmental cues to the next generation. Birds have become a key model for the study of hormone-mediated maternal effects because the embryo develops outside the mother’s body, facilitating the measurement and manipulation of prenatal hormone exposure. At the same time, birds are excellent models for the integration of both proximate and ultimate approaches, which is key to a better understanding of the evolution of hormone-mediated maternal effects. Over the past two decades, a surge of studies on hormone-mediated maternal effects has revealed an increasing number of discrepancies. In this review, we discuss the role of the environment, genetic factors and social interactions in causing these discrepancies and provide a framework to resolve them. We also explore the largely neglected role of the embryo in modulating the maternal signal, as well as costs and benefits of hormone transfer and expression for the different family members. We conclude by highlighting fruitful avenues for future research that have opened up thanks to new theoretical insights and technical advances in the field

Combining GWAS and FST-based approaches to identify targets of Borrelia-mediated selection in natural rodent hosts

This is the author accepted manucript. The final version is available from Wiley via the DOI in this recordData accessibility: The Genotyping-by-Sequencing data are deposited in NCBI BioProject PRJNA306409, SRA experiment SRR3031372. The quality filtered SNP file used for population genomic analyses and information on population and infection status of individual bank voles are deposited in the Dryad repository doi:10.5061/dryad.c866t1g3tRecent advances in high-throughput sequencing technologies provide opportunities to gain novel insights into the genetic basis of phenotypic trait variation. Yet to date, progress in our understanding of genotype-phenotype associations in non-model organisms in general and natural vertebrate populations in particular has been hampered by small sample sizes typically available for wildlife populations and a resulting lack of statistical power, as well as a limited ability to control for false positive signals. Here we propose to combine a genome-wide association (GWAS) and FST-based approach with population-level replication to partly overcome these limitations. We present a case study in which we used this approach in combination with Genotyping-by-Sequencing (GBS) SNP data to identify genomic regions associated with Borrelia afzelii resistance or susceptibility in the natural rodent host of this Lyme disease-causing spirochete, the bank vole (Myodes glareolus). Using this combined approach we identified four consensus SNPs located in exonic regions of the genes Slc26a4, Tns3, Wscd1 and Espnl, which were significantly associated with the voles’ Borrelia infectious status within and across populations. Functional links between host responses to bacterial infections and most of these genes have previously been demonstrated in other rodent systems, making them promising new candidates for the study of evolutionary host responses to Borrelia emergence. Our approach is applicable to other systems and may facilitate the identification of genetic variants underlying disease resistance or susceptibility, as well as other ecologically relevant traits, in wildlife populations.University of Zuric

Interactive and Long-term Effects of Yolk Androgens and Antioxidants in Birds

This is the author accepted manuscript. The final version is available from OUP via the DOI in this recordPoster abstract - Annual Meeting of the Society-for-Integrative-and-Comparative-Biology (SICB), 4-8 January 2017, New Orleans, US

Artificial selection reveals the energetic expense of producing larger eggs

This is the final version of the article. Available from BioMed Central via the DOI in this record.BACKGROUND: The amount of resources provided by the mother before birth has important and long-lasting effects on offspring fitness. Despite this, there is a large amount of variation in maternal investment seen in natural populations. Life-history theory predicts that this variation is maintained through a trade-off between the benefits of high maternal investment for the offspring and the costs of high investment for the mother. However, the proximate mechanisms underlying these costs of reproduction are not well understood. Here we used artificial selection for high and low maternal egg investment in a precocial bird, the Japanese quail (Coturnix japonica) to quantify costs of maternal reproductive investment. RESULTS: We show that females from the high maternal investment lines had significantly larger reproductive organs, which explained their overall larger body mass, and resulted in a higher resting metabolic rate (RMR). Contrary to our expectations, this increase in metabolic activity did not lead to a higher level of oxidative damage. CONCLUSIONS: This study is the first to provide experimental evidence for metabolic costs of increased per offspring investment.The study was financially supported by the Swiss National Science Foundation (PP00P3 128386 and 458 PP00P3 157455 to BT)

Matrilineal inheritance of a key mediator of prenatal maternal effects

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this record.Sex-linkage is predicted to evolve in response to sex-specific or sexually antagonistic selection. In line with this prediction, most sex-linked genes are associated with reproduction in the respective sex. In addition to traits directly involved in fertility and fecundity, mediators of maternal effects may be predisposed to evolve sex-linkage, because they indirectly affect female fitness through their effect on offspring phenotype. Here, we test for sex-linked inheritance of a key mediator of prenatal maternal effects in oviparous species, the transfer of maternally derived testosterone to the eggs. Consistent with maternal inheritance, we found that in Japanese quail (Coturnix japonica) granddaughters resemble their maternal (but not their paternal) grandmother in yolk testosterone deposition. This pattern of resemblance was not due to non-genetic priming effects of testosterone exposure during prenatal development, as an experimental manipulation of yolk testosterone levels did not affect the females' testosterone transfer to their own eggs later in life. Instead, W chromosome and/or mitochondrial variation may underlie the observed matrilineal inheritance pattern. Ultimately, the inheritance of mediators of maternal effects along the maternal line will allow for a fast and direct response to female-specific selection, thereby affecting the dynamics of evolutionary processes mediated by maternal effects.The study was financially supported by Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (PP00P3_128386 and PP00P3_157455) and Fonds zur Förderung des akademischen Nachwuchses (FAN)

The effect of manipulated prenatal conditions on growth, survival, and reproduction throughout the complete life course of a precocial bird

This is the final version. Available on open access from Frontiers Media via the DOI in this record. Data Availability Statement: The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.The quality of the environment individuals experience during development is commonly regarded as very influential on performance in later life. However, studies that have experimentally manipulated the early-life environment and subsequently measured individual performance in all components of fitness over the complete life course are scarce. In this study, we incubated fertile eggs of Japanese quail (Coturnix japonica) at substandard and standard incubation temperature, and monitored growth, survival, and reproduction throughout the complete life course. While embryonic development was slower and hatching success tended to be lower under substandard incubation temperature, the prenatal treatment had no effect on post-hatching growth, survival to sexual maturity, or age at first reproduction. In adulthood, body mass and investment in individual egg mass peaked at middle age, irrespective of the prenatal treatment. Individual reproduction rate declined soon after its onset, and was higher in females that lived longer. Yet, reproduction, and its senescence, were independent of the prenatal treatment. Similarly, adult survival over the complete lifespan was not affected. Hence, we did not find evidence for effects on performance beyond the developmental period that was manipulated. Our results suggest that effects of unfavorable developmental conditions on individual performance later in life could be negligible in some circumstances.Deutsche Forschungsgemeinschaft (DFG

In ovo yolk carotenoid and testosterone levels interactively influence female transfer of yolk antioxidants to her eggs

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this recordMothers can influence prenatal conditions by varying the amount of nutrients, hormones or antioxidants they provide to their developing young. Some of these substances even affect the transfer of these compounds in the next generation, but it is less clear how different maternally transmitted compounds interact with each other to shape reproductive resource allocation in their offspring. Here, we found that female Japanese quail that were exposed to high carotenoid levels during embryonic development transferred lower concentrations of yolk antioxidants to their own eggs later in life. This effect disappeared, when both testosterone and carotenoid concentrations were manipulated simultaneously, showing long-term and interactive effects of these maternally derived egg components on a female’s own egg composition. Given that exposure to high levels of testosterone during embryo development stimulates the production of reactive oxygen (ROS) and impairs antioxidant defenses, we propose that carotenoids act as in-ovo antioxidants in an oxidatively stressful environment (i.e. when levels of testosterone are high) but might have prooxidant properties in an environment where they are not used to counteract an increased production of ROS. In line with this hypothesis, we previously showed that prenatal exposure to increased concentrations of yolk carotenoids leads to a rise of oxidative damage at adulthood, but only when yolk testosterone concentrations were not experimentally increased as well. As a consequence, antioxidants in the body may be used to limit oxidative damage in females exposed to high levels of carotenoids during development (but not in females exposed to increased levels of both carotenoids and testosterone), resulting in lower amounts of antioxidants being available for deposition into eggs. Since prenatal antioxidant exposure is known to influence fitness-related traits, the effect detected in this study might have transgenerational consequences.The study was supported by the Swiss National Science Foundation (PP00P3_128386 and PP00P3_157455) and the Fonds zur Förderung des akademischen Nachwuchses