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It is well established that conditions experienced during prenatal development affect postnatal telomere length and dynamics in humans and laboratory animal models. However, we still know little about how prenatal environmental and social conditions shape telomere dynamics in wild animal populations. In the last years, we have performed several experimental studies to elucidate the role played by maternal glucocorticoids and the exposure to prenatal social stressors (e.g. exposure to predator cues) on postnatal telomere length and dynamics in a long-lived seabird species, the Yellow-legged gull (Larus michahellis). The results of these studies show that in contrast to previously thought, mothers may promote longer telomeres in their offspring by mildly increasing the allocation of glucocorticoids into their eggs (i.e. corticosterone). However, the effect of glucocorticoids hormones seems to differ depending on their intensity, origin and duration. Indeed, when late-stage embryos are repeatedly exposed to predator cues, they show increased secretion of glucocorticoids soon after hatching, an effect that was accompanied by a loss of telomere length during the early postnatal development. Together, our results show that embryos are not passive agents against their developmental environment, as their telomere dynamics are influenced by the maternal phenotype and the social cues they are able to integrate during their development.

SEB Conference 2022

Telomeres in the ocean: how pre- and postnatal factors shape telomere dynamics in a colonial long-lived seabird

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2022 will find over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years.
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2022 found over 1500 experimental biologists from across the globe converging on the third-largest French city near the Mediterranean coast and the fastest-growing city in the country over the past 25 years - Montpellier, France.

Modifications in the cytochrome c oxidase 2 gene of male-transmitted genome (Mcox2) have been found in some bivalve species that exhibit a unique mode of mitochondrial transmission named doubly uniparental inheritance (DUI). In DUI, paternal mitochondria (and their male mtDNA) as well as maternal mitochondria (and their corresponding female mtDNA) are transmitted to male offspring. Scrobicularia plana, a bivalve exhibiting this inheritance model possess an important in-frame insertion of ~ 4,8 kb in its Mcox2 gene that is translated into a polypeptide of 1892 amino acids (~ 220 kDa), the largest metazoan COX2 protein known to date. The insertion is conserved amongst individuals from different populations and, according to analysis of synonymous and non-synonymous substitution rates, evolves under purifying selection which would suggest maintenance of functionality in MCOX2. MCOX2 protein might act as a tag at the surface of male mitochondria to facilitate their sex-specific fate in bivalve embryos. The long-transcribed insertion could also explain low OXPHOS rates that were found in M mitochondria of DUI bivalves thus affecting male mitochondrial metabolism.

Mcox2 in the DUI bivalve Scrobicularia plana encodes the longest known mitochondrial protein in metazoans

Recent cross-sectional comparisons of telomere lengths, a hallmark of ageing, suggest that high temperatures may increase the rate of senescence in ectotherms. Telomeres shorten as a result of exposure to ROS produced by the mitochondria. Given that the rate of ROS production varies with mitochondrial efficiency, there may be a link between an individual’s mitochondrial efficiency and its telomere dynamics, which may be more acute at high temperatures. We tested this hypothesis by examining the relationship between telomere length and mitochondrial function from white muscle and liver of brown trout Salmo trutta of similar age and size, fed ad libitum, and acclimated to high-constant (19.5°C), high-variable (19.5 ± 2.5°C, daily cycle), or ideal (12°C) temperature regimes. Fish under high-constant and high-variable temperature regimes had greater higher average rates of telomere attrition, mitochondrial oxygen consumption rates, and ROS release rates along with lower mitochondrial phosphorylation efficiencies when compared to 12°C acclimated fish. However, telomere changes were positively correlated with mitochondrial phosphorylation efficiency in muscle, but not liver, in fish from the high-constant and high-variable temperature regimes: telomeres shortened in the least efficient individuals but increased in length in the most efficient fish. No relationship was observed in fish acclimated to 12°C. Therefore, individual diversity in muscle mitochondrial efficiency seems to cause variation in cellular senescence, where less efficient individuals have a more rapid shortening of telomeres. This may ultimately suggest that less efficient individuals will have shorter lifespans in warming and fluctuating environments.

Lower muscle mitochondrial efficiency results in more rapid shortening of telomeres in ectotherms at high and fluctuating temperatures

Climate change is increasing both the average ambient temperature and the frequency and severity of heat waves. While direct mortality induced by heat waves is increasingly reported, sub-lethal effects are also likely to impact population dynamics and persistence. We hypothesized that accelerated cellular ageing could be a cost of being exposed to higher ambient temperature. We tested this hypothesis in two common European passerine species by experimentally increasing nest box temperature by ca. 2°C during postnatal growth and measuring telomere length as a biomarker of ageing. In great tits, we also estimated the impact on medium-term survival and measured a large set of physiological markers including thyroid hormones, glucocorticoid signaling, oxidative stress, mitochondrial density and telomere maintenance mechanisms. We show that in both species, increasing early-life temperature does not affect growth or survival to fledging, but leads to an acceleration in the shortening of telomeres. In great tits, such shortening of telomeres was not explained by increased oxidative stress levels, but more likely by an increase in energy demand (i.e. higher thyroid hormones levels, increased expression of glucocorticoid receptor, increased mitochondrial density) leading to a reduction in telomere maintenance mechanisms (i.e. decrease in the gene expression of telomerase and protective shelterin). Additionally, medium-term survival was reduced from 34% in control nests to 19% in heated nests. Our results thus suggest that climate warming might affect cellular ageing in wild passerine populations, with potential impact on population dynamics and persistence.

From climate warming to accelerated cellular ageing: insights from two experimental studies in wild passerine birds

Individual variation in telomere length has been linked with health, survival and senescence. Individual variation in telomere length is due to environmental and genetic effects, which can be partitioned into their relative variance components. Estimating the ratio of additive genetic variance to the total phenotypic variance of telomere length, known as the heritability of telomere length, then facilitates understanding of the evolutionary potential of telomere length. However, telomere length heritability estimates vary greatly, and there is a limited understanding of why this is. To fill this knowledge gap, we conducted a systematic review and meta-analysis. We extracted 104 estimates from 43 studies and 18 species to test whether variation in telomere length heritability estimates is due to: phylogeny, species, environmental setting, age at sampling, laboratory methods, statistical methods, and individual repeated measurements. Overall, we found a moderate heritability of 45% (95% CI: 25% – 65%), and significant phylogenetic and species-specific effects, suggesting differential selection pressures on telomere length across taxa. Twin-based and SNP-based estimates were lower than correlation-based or pedigree-based estimates. Furthermore, we detected a publication bias, where small studies with low or non-significant heritability were under-represented. Our results demonstrate an overall heritable basis of telomere length, and the need for careful selection of statistical methods. Specifically, we recommend variance-partitioning methods with relatedness or SNP data over correlation methods to minimize bias. We also recommend future research to expand into a wider range of taxa, and to explore and validate the use of genome-wide correlation data in calculating quantitative genetic metrics.

Heritability of telomere length: a meta-analysis

The disposable soma theory predicts that ageing is a consequence of the investment in reproduction at the expense of self-maintenance. Depending on their pace of life (POL), individuals prioritise either reproduction (fast POL) or self-maintenance (slow POL). A fast POL is associated with a rapid accumulation of physiological damage and early death, and vice versa for a slow POL. To date, especially in vertebrates, it is unclear if physiological damage accumulates uniformly across the entire body, or if there are within-body mosaics of ageing. Here, we quantified telomere length (TL) by TRF in blood, spleen and reproductive tissue in Japanese quail (Coturnix japonica) artificially selected for high (fast POL) or low (slow POL) reproductive investment to test for POL-dependent within-body mosaics of ageing. We found that TL differed across reproductive and non-reproductive tissues in a sex-specific way, but found no indication that these within-body mosaics of TL were affected by an individual’s POL. In females telomeres were longer in oviduct than in blood or spleen, whereas in males TL in testes was not different from TL in non-reproductive tissues, but telomeres in spleen were longer than telomeres in blood. Our study provides evidence for sex-specific within-body mosaic of ageing, which are, however, independent of an individual’s life history strategy.

Do life history strategies affect within-body mosaics of ageing?

Despite ~80% of all animal species undergoing metamorphosis, the effect of this dramatic developmental process on telomere dynamics is unknown. Given that the rate of telomere shortening has been shown in non-metamorphosing species to be influenced by environmental harshness, the question arises as to whether the re-modelling of tissues that occurs during metamorphosis allows an individual to re-set its telomeres and so leave behind this legacy of past environments. This issue is pertinent to amphibians, a group likely to be heavily impacted in the larval stage (i.e., before metamorphosis) by environmental events such as global warming. We will first briefly discuss the current knowledge gaps in the study of amphibian telomeres, then present new data on telomere length across different tissues and developmental stages (from larva to adulthood) in the frog Xenopus laevis. We will also examine the impact of warming conditions before and after metamorphosis on amphibian telomeres and telomerase. Our results show that telomere length is affected not only by the rate of somatic growth, but also by the degree of metamorphic transformation experienced by particular tissues: during metamorphosis, telomere length can either decline, remain stable or dramatically increase. Furthermore, this life history transition seems to be able to buffer the impact on telomeres of harsh conditions in early life. This leads us to suggest directions for future research on telomere dynamics in amphibians and other species with complex-life cycles.

Across the great divide: telomere dynamics through metamorphosis in amphibians

Genomics provide researchers with solutions to better predict the phenotypic characteristics, economic value and adaptive potential of species, and improves our understanding of the diversity present in wild populations. I will reflect on our work to develop high-quality genome assemblies and associated analyses for plant and animal species of importance to New Zealand (Aotearoa), including species that are considered as treasures (taonga) by indigenous Māori people. Specifically, I will present my perspectives and experiences as a European biologist who works in a government-owned research institution, alongside Māori communities, academics and commercial enterprises, to reflect on my journey to achieve positive impact and shared benefits with Māori using genomics research.

Plant and animal genomics research for and with indigenous communities: a European scientist’s perspective.

Examining global patterns of DSI sharing and use to inform policy

Recent changes to the legal frameworks regulating genetic resources -- including the expanding reach of ABS under the Nagoya Protocol,  and the growing number of non-State institutions developing their own ABS schemes – are having a negative impact on the collection, transfer, and use of genetic resources. The talk argues that while these are challenging issues that the stakes are too high not to attempt to find a solution, and that there is potential for researcher driven solutions to the legal uncertainty created by the Nagoya Protocol.  

Nagoya Protocol and access to genetic resources

Concerns over Indigenous Data Sovereignty and Indigenous rights under the Nagoya Protocol underpin the development and application of Traditional Knowledge and Biocultural Labels/Notices. The Local Contexts system which delivers the Labels and Notices, is focused on implementing Indigenous provenance, protocols, and permissions into digital infrastructures. The Labels and Notices are designed to provide a persistent and durable connection between collaborating Indigenous communities and researchers, research projects, genetic resources, Digital Sequence Information (DSI), and associated traditional knowledge, that exist as metadata in sample/data repositories. The Biocultural Labels support Nagoya Protocol expectations around the disclosure and origins of genetic resources (i.e. Provenance Label) and help to define and communicate Indigenous community expectations and consent about appropriate and future use of genetic resources and derived benefits. Importantly BC Labels may only be applied by an Indigenous community, and they are both human readable and machine readable. The Notices are a distinct tool for researchers who can use this mechanism to disclose Indigenous rights and interests. This presentation will introduce the Labels and Notices and explore the responsibilities that universities and researchers have to practically implement mechanisms that enable transparency around Indigenous rights and interests in support of Indigenous Data Sovereignty.

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Mcox2 in the DUI bivalve Scrobicularia plana encodes the longest known mitochondrial protein in metazoans

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Mcox2 in the DUI bivalve Scrobicularia plana encodes the longest known mitochondrial protein in metazoans

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