Maternal testosterone affects offspring telomerase activity in a long-lived seabird

Noguera, J.C. and Velando, A., 2022. Maternal testosterone affects offspring telomerase activity in a long‐lived seabird. Ecology and Evolution, 12(9), p.e9281.

Androgens are a group of steroid hormones that have long been proposed as a mechanism underpinning intergenerational plasticity. In birds, maternally allocated egg testosterone, one of the main androgens in vertebrates, affects a wide variety of offspring phenotypic traits but the mechanisms underlying this form of intergenerational plasticity are not yet well understood. Recent in vitro and animal model studies have shown that telomerase expression and activity are important targets of androgen signaling. The telomerase enzyme is known for its repair function on telomeres, the DNA–protein complexes at the ends of chromosomes that are involved in genomic integrity and cell aging. However, the role of maternal testosterone in influencing offspring telomerase levels in natural populations and its consequences on telomere length and potentially on offspring development is still unknown. Here, by experimentally modifying the level of egg testosterone in a natural population of yellow-legged gull (Larus michahellis), we show that chicks hatched from testosterone-treated eggs had higher average levels of telomerase and faster growth than controls during the first week of life. While testosterone-treated chicks also tended to have longer telomeres than controls at hatching this difference disappeared by day 6 of age. Overall, our results suggest that maternal testosterone may have a potential adaptive value by promoting offspring growth and presumably telomerase levels, as this enzyme plays other important physiological functions (e.g., stress resistance, cell signaling, or tissue genesis) besides telomere lengthening. Nonetheless, our knowledge of the potential adaptive function of telomerase in natural populations is scarce and so the potential pathways linking maternal hormones, offspring telomerase, and fitness should be further investigated.

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Egg corticosterone can stimulate telomerase activity and promote longer telomeres during embryo development

Noguera, J.C., da Silva, A. and Velando, A., Egg corticosterone can stimulate telomerase activity and promote longer telomeres during embryo development. Molecular Ecology. https://doi.org/10.1111/mec.15694


It is often assumed that the transfer of maternal glucocorticoids (GCs; e.g. corticosterone or cortisol) to offspring is an inevitable cost associated with adverse or stressful conditions experienced by mothers. However, recent evidence indicates that maternal GCs may adaptively program particular physiological and molecular pathways during development to enhance offspring fitness. In this context, an important mechanism through which maternal GCs may lastingly affect offspring phenotypic quality and survival is via effects on embryo telomerase activity and so on offspring postnatal telomere length. Here, using a field experimental design for which we manipulated the corticosterone content in yellow‐legged gull (Larus michahellis) eggs, we show that embryos from corticosterone‐injected eggs not only had a higher telomerase activity but also longer telomeres just after hatching. A complementary analysis further revealed that gull hatchlings with longer telomeres had a higher survival probability during the period when most of the chick mortality occurs. Given the important role that telomere length and its restoring mechanisms have on ageing trajectories and disease risk, our findings provide a new mechanistic link by which mothers may presumably shape offspring life‐history trajectories and phenotype.


https://doi.org/10.1111/mec.15694

Maternal programming of offspring antipredator behavior in a seabird

Morales, J., Lucas, A. e Velando, A., 2018. Maternal programming of offspring antipredator behavior in a seabird. Behavioral Ecology, arx197, https://doi.org/10.1093/beheco/arx197


Predation risk is an important environmental factor for animal populations, expected to trigger maternal effects to prepare offspring for living in an environment with predators. Yet, evidence of adaptive anticipatory maternal effects in wild animals is still weak. Here, we explored this question in a wild colony of yellow-legged gulls, Larus michahellis. To this aim, prior to laying we exposed mothers to either mink decoys or nonpredator rabbit decoys and explored the antipredator behavior of 118 chicks at the age of 2 days. We found that chicks from second-laid eggs by predator-exposed mothers crouched faster after hearing a playback with adult alarm calls than chicks from second-laid eggs by control mothers. Besides, chicks from third-laid eggs by predator-exposed mothers were lighter than control chicks, but this was not due to differences in egg volume. Our results suggest that predator-exposed mothers modified offspring phenotype via eggs to cope with predators, although only in chicks from second-laid eggs. Maternal transference of corticosterone could underlie chick behavioral plasticity. Results support the role of maternal effects as a form of phenotype programming to forewarn offspring about environmental hazards.

Hatching hierarchy but not egg-related effects governs behavioral phenotypes in gull chicks

Diaz-Real, J., Kim, S.Y. & Velando, A., 2016. Hatching hierarchy but not egg-related effects governs behavioral phenotypes in gull chicks. Behavioral Ecology. doi: 10.1093/beheco/arw110


In many bird species that practice parental care, siblings often compete for resources and care provided by their parents, although their strategies differ according to hatching rank and condition. Differences in offspring strategies are generally attributed to hatching order and maternal effects, which are difficult to separate because these effects are often correlated. For example, third-hatched chicks of large gull species receive more egg testosterones and corticosterone, which influence early behavioral patterns. In this study, we carried out a cross-fostering experiment with first- and last-laid eggs of the yellow-legged gull (Larus michahellis) to test whether the within-brood variation in behavioral strategies for competing with siblings and coping with stress are due to maternal effects or to hatching order. Chicks hatched in the last position within the experimental brood emitted more chatter calls to attract parents’ attention, were less prone to respond to warning of danger, and had a lower breathing rate while restrained than first-hatched chicks. Egg laying order did not affect chick behaviors or breathing rate. Thus, we concluded that the different behavioral strategies of chicks were determined by their posthatching experience and not by the original egg position within the clutch. Last-laid eggs were smaller and chicks from those eggs grew slower than chicks from first-laid eggs. Independently of the original laying order, chicks that hatched first in the experimental brood grew faster than their siblings. Overall, our results indicate that behavioral strategies of chicks are plastic and influenced by their early social

Maternal testosterone influences a begging component that makes fathers work harder in chick provisioning

Noguera, J. C., Kim, S.-Y. & Velando, A. Maternal testosterone influences a begging component that makes fathers work harder in chick provisioning. Hormones and behavior 64, 19–25 (2013).


In species with biparental care, parents disagree evolutionarily over the amount of care that each of them is willing to provide to offspring. It has recently been hypothesised that females may try to manipulate their mates by modifying offspring begging behaviour through yolk hormone deposition, shifting the division of labour in their own favour. To test this hypothesis we first investigated how yellow-legged gull (Larus michahellis) parents feed offspring in relation to each component of complex begging behaviour and if feeding behaviour varies between sexes. Then we investigated the effect of yolk testosterone on chicks’ begging by experimentally increasing yolk testosterone levels. Our results revealed that yolk testosterone has a component-specific effect on chicks’ begging, specifically increasing the number of chatter calls. Parental feeding effort was influenced by the number of chatter calls emitted by chicks, but most importantly, the influence was stronger in male than in female parents. Moreover, chick body mass increased with the number of paternal feeds. In conclusion, these results show that female gulls may use yolk testosterone deposition to exploit their partners as predicted by the ‘Manipulating Androgen Hypothesis (MAH)’.