Biology subjects

Ruuskanen, S.

Publications and source records attributed to Ruuskanen, S..

34 records · Page 2Linked to original sources

bioRxiv2021

Prenatal thyroid hormones accelerate postnatal growth and telomere shortening in wild great tits

Early-life environment is known to affect later-life health and disease, which could be mediated by the early-life programming of telomere length, a key hallmark of ageing. According to the fetal programming of telomere biology hypothesis, variation in prenatal exposure to hormones is likely to influence telomere length. Yet the contribution of key metabolic hormones, i.e. thyroid hormones (THs), has been largely ignored. We recently showed that in contrast to predictions, exposure to elevated prenatal THs increased postnatal telomere length in wild collared flycatchers, but the generality of such effect, its underlying proximate mechanisms and consequences on survival have not been investigated. We therefore conducted a comprehensive study evaluating the impact of THs on potential drivers of telomere dynamics (growth, post-natal THs, mitochondria and oxidative stress), telomere length and medium-term survival using wild great tits as a model system. While prenatal THs did not significantly affect telomere length a week after hatching (i.e. day 7), they influenced postnatal telomere shortening (i.e. shorter telomeres at day 14 and the following winter) but not apparent survival. Circulating THs, mitochondrial density or oxidative stress biomarkers were not significantly influenced, whereas TH-supplemented group showed accelerated growth, which may explain the observed delayed effect on telomeres. We discuss several alternative hypotheses that may explain the contrast with our previous findings in flycatchers. Given that shorter telomeres in early life tend to be carried until adulthood and are often associated with decreased survival prospects, the effects of prenatal THs on telomeres may have long-lasting effects on senescence.

evolutionary biology↗

bioRxiv2021

Altricial bird early-stage embryos express the molecular "machinery" to respond to maternal thyroid hormone cues

Maternal hormones, such as thyroid hormones transferred to embryos and eggs, are key signalling pathways to mediate maternal effects. To be able to respond to maternal cues, embryos must express key molecular machinery of the hormone pathways, such as enzymes and receptors. While altricial birds begin thyroid hormone (TH) production only at/after hatching, experimental evidence suggests that their phenotype can be influenced by maternal THs deposited in the egg. However, it is not understood, how and when altricial birds express genes in the TH-pathway. For the first time, we measured the expression of key TH-pathway genes in altricial embryos, using two common altricial ecological model species (pied flycatcher, Ficedula hypoleuca and blue tit Cyanistes caeruleus). Deiodinase DIO1 gene expression could not be reliably confirmed in either species, but deiodinase enzyme DIO2 and DIO3 genes were expressed in both species. Given that DIO2 coverts T4 to biologically active T3, and DIO3 mostly T3 to inactive forms of thyroid hormones, our results suggest that embryos may modulate maternal signals. Thyroid hormone receptor (THRA and THRB) and monocarboxyl membrane transporter gene (SLC15A2) were also expressed, enabling TH-responses. Our results suggest that early altricial embryos may be able to respond and potentially modulate maternal signals conveyed by thyroid hormones.

developmental biology↗

bioRxiv2021

Is maternal thyroid hormone deposition subject to a trade-off between self and egg because of iodine? An experimental study in rock pigeon

Maternal hormones constitute a key signalling pathway for mothers to shape offspring phenotype and fitness. Thyroid hormones (THs; triiodothyronine, T3 and thyroxine, T4) are metabolic hormones known to play crucial roles in embryonic development and survival in all vertebrates. During early developmental stages, embryos exclusively rely on the exposure to maternal THs, and maternal hypothyroidism can cause severe embryonic maldevelopment. The TH molecule includes iodine, an element that cannot be synthesised by the organism. Therefore, TH production may become costly when environmental iodine availability is low. This may yield a trade-off for breeding females between allocating the hormones to self or to their eggs, potentially to the extent that it even influences the number of laid eggs. In this study, we investigated whether low dietary iodine may limit TH production and transfer to the eggs in a captive population of Rock pigeons (Columba livia). We provided breeding females with an iodine-restricted (I- diet) or iodine-supplemented diet (I+ diet) and measured the resulting circulating and yolk iodine and TH concentrations and the number of eggs laid. Our iodine-restricted diet successfully decreased both circulating and yolk iodine concentrations compared to the supplemented diet, but not circulating or yolk THs. This indicates that mothers may not be able to independently regulate hormone exposure for self and their embryos. However, egg production was clearly reduced in the I- group, with fewer females laying eggs. This result shows that restricted availability of iodine does induce a cost in terms of egg production. Whether females reduced egg production to preserve THs for themselves or to prevent embryos from exposure to low iodine and/or THs is as yet unclear.

physiology↗

bioRxiv2020

Does arsenic contamination affect DNA methylation patterns in a wild bird population? An experimental approach

Pollutants, such as toxic metals, negatively influence organismal health and performance, even leading to population collapses. Studies in model organisms have shown that epigenetic marks, such as DNA methylation, can be modulated by various environmental factors, including pollutants, influencing gene expression and various organismal traits. Yet experimental data on the effects of pollution on DNA methylation from wild animal populations is largely lacking. We here experimentally investigated for the first time the effects of early-life exposure to environmentally relevant levels of a key pollutant, arsenic (As), on genome-wide DNA methylation in a wild bird population. We experimentally exposed nestlings of great tits (Parus major) to arsenic during their post-natal developmental period (3 to 14 days post-hatching) and compared their erythrocyte DNA methylation levels to those of respective controls. In contrast to predictions, we found no overall hypomethylation in the arsenic group. We found evidence for loci to be differentially methylated between the treatment groups, but for five CpG sites only. Three of the sites were located in gene bodies of zinc finger and BTB domain containing 47 (ZBTB47), HIVEP zinc finger 3 (HIVEP3) and insulin like growth factor 2 mRNA binding protein 1 (IGF2BP1). Further studies are needed to evaluate whether epigenetic dysregulation is a commonly observed phenomena in polluted populations, and what the consequences are for organism functioning and for population dynamics.

ecology↗

bioRxiv2020

Adaptation of bacteria to glyphosate: a microevolutionary perspective of the enzyme 5-enolpyruvylshikimate 3-phosphate (EPSP) synthase

Glyphosate is the leading herbicide worldwide, but it also affects prokaryotes because it targets the central enzyme (EPSPS) of the shikimate pathway in the synthesis of the three essential aromatic amino acids in autotrophs. Our results reveal that bacteria easily become resistant to glyphosate through changes in the EPSPS active site. This indicates the importance of examining how glyphosate affects microbe-mediated ecosystem functions and human microbiomes.

microbiology↗

bioRxiv2020

Classification of the glyphosate target enzyme (5-enolpyruvylshikimate-3-phosphate synthase)

Glyphosate is the most common broad-spectrum herbicide. It targets the key enzyme of the shikimate pathway, 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), which synthesizes three essential aromatic amino acids (phenylalanine, tyrosine and tryptophan) in plants. Because the shikimate pathway is also found in many prokaryotes and fungi, the widespread use of glyphosate may have unsuspected impacts on the diversity and composition of microbial communities, including the human gut microbiome. Here, we introduce the first bioinformatics method to assess the potential sensitivity of organisms to glyphosate based on the type of EPSPS enzyme. We have precomputed a dataset of EPSPS sequences from thousands of species that will be an invaluable resource to advancing the research field. This novel methodology can classify sequences from >90% of eukaryotes and >80% of prokaryotes. A conservative estimate from our results shows that 54% of species in the core human gut microbiome are sensitive to glyphosate.

bioinformatics↗

bioRxiv2020

Born to be young: prenatal thyroid hormones increase early-life telomere length

Prenatal environmental conditions can have lifelong consequences on health and aging. The underlying mechanisms remain nonetheless little understood. Thyroid hormones (THs) are important regulators of embryogenesis transferred from the mother to the embryo. In an avian model, we manipulated embryo exposure to maternal THs through egg injection and investigated the consequences on postnatal growth and aging. We first report that mitochondrial DNA (mtDNA) copy number and telomere length significantly decrease from early-life to late adulthood, thus confirming that these two molecular markers are hallmarks of aging in our wild bird model. The experimental elevation of prenatal THs levels had a transient positive effect on postnatal growth. Elevated prenatal THs had no effect on mtDNA copy number but significantly increased telomere length both soon after birth and at the end of the growth period (equivalent to offsetting ca. 4 years of post-growth telomere shortening). These findings suggest that prenatal THs have a key role in setting the biological age at birth, and thus might influence longevity.

physiology↗

bioRxiv2020

Testing for context-dependent effects of maternal thyroid hormones on offspring survival and physiology: an experimental approach manipulating temperature in a wild bird species

Maternal effects via hormonal transfer from the mother to the offspring provide a tool to translate environmental cues to the offspring. Experimental manipulations of maternally transferred hormones have yielded increasingly contradictory results, which may be explained by environment-dependent effects of hormones. Yet context-dependent effects have rarely been experimentally tested. We therefore studied whether maternally transferred thyroid hormones (THs) exert context-dependent effects on offspring survival and physiology by manipulating both egg TH levels and post-hatching nest temperature in wild pied flycatchers (Ficedula hypoleuca) using a full factorial design. We found no clear evidence for context-dependent effects of prenatal THs related to postnatal temperature on growth, survival and potential underlying physiological responses (plasma TH levels, oxidative stress and mitochondrial density). We conclude that future studies should test for other key environmental conditions, such as food availability, to understand potential context-dependent effects of maternally transmitted hormones on offspring, and their role in adapting to changing environments.

ecology↗

bioRxiv2020

Testing different forms of regulation of yolk thyroid hormone transfer in pied flycatchers

Hormones transferred from mothers to their offspring are considered a maternal tool to prepare progeny for expected environmental conditions, increasing maternal fitness. To flexibly influence offspring, mothers should be able to transmit the hormonal signals independent of their own hormonal status. However, the ability to regulate hormone transfer to the next generation is under debate. We studied the transfer of thyroid hormones (THs) to eggs in a bird model. We elevated thyroxine (T4, the prohormone for the biological active triiodothyronine, T3) during egg-laying using T4 implants on females of a wild population of pied flycatchers (Ficedula hypoleuca), and measured plasma and yolk T4 and T3 as a response. To our knowledge, studies that manipulated a prohormone and measured the change in its active metabolites have rarely been conducted. We found an increase in plasma and yolk T4 and no change in T3 concentrations leading to a similar decrease in yolk T3/T4 ratio in response to the T4 treatment in plasma and yolk. This suggests that mothers are able to regulate the conversion of T4 in T3 to avoid potential costs of elevated exposure to the active hormone to herself and to her progeny. Finally, contrary to our predictions, we found no evidence of regulatory mechanisms at the follicle level, which is essential for independent regulation of yolk hormone transfer. Summary statementThyroid hormones have been overlooked in the context of hormone-mediated maternal effects. We found that mothers may regulate yolk thyroid hormone transfer by regulating the conversion of the active form of the hormone.

physiology↗

bioRxiv2019

Parental effects via glyphosate-based herbicides in a bird model?

Controversial glyphosate-based herbicides (GBHs) are the most frequently used herbicides across the globe. In an increasing number of studies, researchers have identified GBH residues in soil, water, crops, and food products exposing non-target organisms to health risks; these organisms include wildlife, livestock, and humans. However, GBH-related parental effects are poorly understood. In the case of birds, GBHs may be transferred directly from mother to developing offspring (i.e. direct effects) via eggs, or they may indirectly influence offspring performance by altered maternal condition or resource allocation to eggs, for example. We experimentally exposed a parental generation of Japanese quails (Coturnix japonica) to GBHs or respective controls, recorded egg quality and glyphosate residues in eggs, and studied embryonic development and oxidative biomarkers. Glyphosate accumulated in eggs (ca 0.76 kg/mg). Embryonic development tended to be lower in eggs of GBH-exposed parents compared to control parents. Embryonic brain tissue from GBH-exposed parents tended to express more lipid damage. Given that we detected no differences in egg quality (egg, yolk, or shell mass, or egg hormone concentration) across the treatment groups, our results suggest these are likely direct effects of GBHs on offspring rather than indirect effects via altered maternal allocation of resources or hormonal signals. CapsuleExperimental, long-term parental exposure to GBHs tends to hinder offspring embryonic development and increase embryonic oxidative damage to lipids in a bird model.

pharmacology and toxicology↗

bioRxiv2019

The effect of experimental lead pollution on DNA methylation in a wild bird population

Anthropogenic pollution is known to negatively influence an organisms physiology, behavior and fitness. Epigenetic regulation, such as DNA methylation, has been hypothesized as one mechanism to mediate such effects, yet studies in wild species are lacking. We first investigated the effects of early-life exposure to the heavy metal lead (Pb) on DNA methylation levels in a wild population of great tits (Parus major), by experimentally exposing nestlings to lead at environmentally relevant levels. Secondly, we studied the effects of heavy metal exposure in a population close to a copper smelter, where birds suffer from pollution-related decrease in food quality. For both comparisons, the analysis of about million CpGs covering most of the annotated genes, revealed that regions enriched for developmental processes showed pollution-related changes in DNA methylation, but the results were not consistent with binomial and beta binomial regression. Our study indicates that post-natal anthropogenic heavy metal exposure can affect methylation levels of development related genes in a wild bird population.

molecular biology↗

bioRxiv2019

Inter-specific variation of maternal thyroid hormones associate with migration, mode of development, and captivity: a phylogenetic comparative analysis

Life-history traits vary largely across species and several physiological parameters have been proposed to be associated with life-history variation, such as metabolic rates, glucocorticoids, and oxidative stress. Interestingly, the association between thyroid hormones (THs) and life history variation has never been considered, despite a close interaction between THs and these physiological traits. Because of the crucial effects on embryonic development, THs can also induce transgenerational plasticity when transferred to developing offspring, for instance, via egg yolks in birds. In this study, we compiled a unique data set of maternal yolk THs in 34 bird species across 17 families and 6 orders, and tested for associations with various life-history traits. Our phylogenetic mixed models indicated that both concentrations and total amounts of the two most important forms of THs (T3 and T4) were higher in the eggs of migratory species than in those of resident species, and that there were higher total amounts of T3 in the eggs of precocial species than in those of altricial species. However, maternal THs did not show clear associations with any traits of the pace-of-life syndrome, such as developmental duration, growth rate, or lifespan. When taking environmental factors into account, we found that captive species deposited higher TH concentrations and larger amounts in the egg yolks than wild species. These findings suggest that maternal THs are likely involved in the evolution of life-history variation, or vice versa.

evolutionary biology↗

bioRxiv2019

Elevated exposure to prenatal thyroid hormones affects embryonic mortality but has no effects into adulthood

Maternal thyroid hormones (THs) are known to be crucial in embryonic development in humans, but their influence on other, especially wild, animals remains poorly understood. So far, the studies that experimentally investigated the consequences of maternal THs focused on short-term effects, while early organisational effects with long-term consequences, as shown for other prenatal hormones, could also be expected. In this study, we aimed at investigating both the short- and long-term effects of prenatal THs in a bird species, the Japanese quail Coturnix japonica. We experimentally elevated yolk TH content (the prohormone T4, and its active metabolite T3, as well as a combination of both hormones). We analysed hatching success, embryonic development, offspring growth and oxidative stress as well as their potential organisational effects on reproduction, moult, and oxidative stress in adulthood. We found that eggs injected with both hormones had a higher hatching success compared with control eggs, suggesting conversion of T4 into T3 by the embryo. We detected no other clear short-term or long-term effects of yolk THs. These results suggest that yolk thyroid hormones are important in the embryonic stage of precocial birds, but other short- and long-term consequences remain unclear. Research on maternal thyroid hormones will greatly benefit from studies investigating how embryos use and respond to this maternal signalling. Long-term studies on prenatal THs in other taxa in the wild are needed for a better understanding of this hormone-mediated maternal pathway.

physiology↗

bioRxiv2019

Transgenerational endocrine disruption? Experimental copper exposure, but not heat stress, leads to elevated egg thyroid hormone levels

Climate change and pollution are some of the greatest anthropogenic threats to wild animals. Transgenerational plasticity - when parental exposure to environmental stress leads to changes in offspring phenotype - has been recently highlighted as a potential mechanism to respond to various environmental and anthropogenic changes across taxa. Transgenerational effects may be mediated via multiple mechanisms, such as transfer of maternal hormones to eggs/fetus. However, sources of variation in hormone transfer are poorly understood in fish, and thus the first step is to characterize whether environmental challenges alter transfer of maternal hormones to eggs. To this end, we explored the genetic and environmental variation (in response to temperature and endocrine disrupting copper) in maternal thyroid hormone (TH), transfer to offspring in a common fish model species, the three-spined stickleback (Gasterosteus aculeatus) using multiple approaches: (i) We compared ovarian TH levels among six populations across a wide geographical range in the Baltic Sea, including two populations at high water temperature areas (discharge water areas of nuclear power plants) and we experimentally exposed fish to (ii) environmentally relevant heat stress and (iii) copper for 7 days. We found that populations did not differ in intraovarian TH levels, and short-term heat stress did not influence intraovarian TH levels. However, copper exposure increased both T4 and T3 levels in ovaries. The next step would be to evaluate if such alterations would lead to changes in offspring phenotype. Capsule: We show that experimental copper exposure, but not heat stress (experimental or among-population variation), leads to elevated ovarian thyroid hormone levels in sticklebacks.

physiology↗

bioRxiv2019

Plastic but repeatable: rapid adjustments of mitochondrial function and density during reproduction in a wild bird species

Most of the energy fluxes supporting animal performance flow through mitochondria. Hence, inter-individual differences in performance might be rooted in inter-individual variations in mitochondrial function and density. Furthermore, because the energy required by an individual often changes across life stages, mitochondrial function and density are also expected to show within-individual variation (i.e. plasticity). No study so far has repeatedly measured mitochondrial function and density in the same individuals to simultaneously test for within-individual repeatability and plasticity of mitochondrial traits. Here, we repeatedly measured mitochondrial DNA copy number (a proxy of density) and respiration rates from blood cells of female pied flycatchers (Ficedula hypoleuca) at the incubation and chick-rearing stages. Mitochondrial density and respiration rates were all repeatable (R = [0.45-0.80]), indicating high within-individual consistency in mitochondrial traits across life-history stages. Mitochondrial traits were also plastic, showing a quick (i.e. 10 days) down-regulation from incubation to chick-rearing in mitochondrial density, respiratory activity, and cellular regulation by endogenous substrates and/or ATP demand. These downregulations were partially compensated by an increase in mitochondrial efficiency at the chick-rearing stage. Therefore, our study provides clear evidence for both short-term plasticity and high within-individual consistency in mitochondrial function and density during reproduction in a wild bird species.

physiology↗

bioRxiv2019

Prenatal thyroid hormone exposure increases growth but not oxidative stress in a wild passerine species

Hormones transferred from mothers to their offspring are thought to be a maternal tool for mothers to prepare their progeny for expected environmental conditions, thus increasing fitness. Thyroid hormones (THs) are crucial across vertebrates for embryonic and post-natal development and metabolism. Nevertheless, the studies that investigated the consequences of maternal hormones have mostly focused on steroid hormones and ignored maternally-derived thyroid hormones. In this study, we experimentally elevated yolk thyroid hormones in a wild population of a migratory passerine, the European Pied flycatcher Ficedula hypoleuca. We injected eggs with a mixture of T4 and T3 within the natural range of the species to assess its effects on hatching success, nestling survival, growth and oxidative status (antioxidant enzyme activity, lipid peroxidation and oxidative balance). We found no effects of yolk THs on egg hatchability or nestling survival. Yolk THs increased nestling growth during the second week post hatching, but this potentially beneficial effect did not incur any costs in terms of oxidative stress. The results should stimulate more research on thyroid hormone mediated maternal effects, further studies into the underlying mechanistic pathways for these effects and how they translate into adulthood and fitness.\n\nSummary statementThyroid hormones have been overlooked in the context of hormone-mediated maternal effects. We found that yolk thyroid hormones in a wild bird species increase growth without incurring oxidative stress.

physiology↗