The increasing number of reported cases of antibiotic resistance is one of today’s major public health concerns. Dealing with this threat involves understanding what drives the evolution of antibiotic resistance and investigating whether we can predict (and subsequently avoid or circumvent) it [1].
One of the most illustrative and common models of adaptation (and, hence, resistance evolution) is Fisher’s Geometric Model (FGM). The original model maps phenotypes to fitness, meaning that each point in the fitness landscape corresponds to a phenotype rather than a genotype. However, it has been shown that when mutations are numerous enough, FGM can also describe adaptive walks in genotype space [2]. Nevertheless, limitations have been highlighted, particularly when trying to study complex scenarios such as antibiotic resistance evolution [3].
Harmand et al. [4] incorporated three extensions to the FGM, which allowed them to match the mutational patterns of antibiotic resistance that they obtained from a screen across a gradient of drug concentrations. The implemented extensions took into account that: 1) only a subset of mutations may contribute to traits under selection, reflecting that not all regions in the genome affect the ability to resist antibiotics; 2) mutations that confer a fitness increase in one environment may not reflect a similar increase in others, if the selective constraints are different; and 3) different antibiotic concentrations may either constrain the maximum fitness that populations can reach (changing the height of the fitness peak) or change the rate of fitness increase with each mutation (changing the width/slope of the peak).
Traditionally, most empirical fitness landscape studies have focused on a subset of mutations obtained after laboratory evolution in specific conditions [5, 6]. The results obtained in Harmand et al. [4] indicate a potential shortcoming of studying these small fitness landscapes: rather than having a constrained evolutionary path to a resistant phenotype, as previously observed, their results suggest that antibiotic resistance can be the product of mutations in different regions of the genome. Returning to the fitness landscape perspective, this indicates that there are many alternative paths that can lead to the evolution of antibiotic resistance. This comparison points at a difficult challenge when aiming at developing a predictive framework for evolution: real-time experiments may indicate that evolution is likely to take similar and predictable paths because the strongest and most frequent mutations dictate the outcome, whereas systematic screens of mutants potentially indicate several paths, that may, however, not be relevant in nature. Only a combination of different experimental approaches with motivated theory as presented in Harmand et al. [4] will allow for a better understanding of where in this continuum evolution is taking place in nature, and to which degree we are able to interfere with it in order to slow down adaptation.

References

[1] Palmer AC, and Kishony R. 2013. Understanding, predicting and manipulating the genotypic evolution of antibiotic resistance. Nature Review Genetics 14: 243—248. doi: 10.1038/nrg3351

[2] Tenaillon O. 2014. The utility of Fisher’s geometric model in evolutionary genetics. Annual Review of Ecology, Evolution and Systematics 45: 179—201. doi: 10.1146/annurev-ecolsys-120213-091846

[3] Blanquart F and Bataillon T. 2016. Epistasis and the structure of fitness landscapes: are experimental fitness landscapes compatible with Fisher’s geometric model? Genetics 203: 847—862. doi: 10.1534/genetics.115.182691

[4] Harmand N, Gallet R, Jabbour-Zahab R, Martin G and Lenormand T. 2017. Fisher’s geometrical model and the mutational patterns of antibiotic resistance across dose gradients. Evolution 71: 23—37. doi: 10.1111/evo.13111

[5] de Visser, JAGM, and Krug J. 2014. Empirical fitness landscapes and the predictability of evolution. Nature 15: 480—490. doi: 10.1038/nrg3744

[6] Palmer AC, Toprak E, Baym M, Kim S, Veres A, Bershtein S and Kishony R. 2015. Delayed commitment to evolutionary fate in antibiotic resistance fitness landscapes. Nature Communications 6: 1—8. doi: 10.1038/ncomms8385

Biological invasions are natural experiments, and often show that evolution can affect dynamics in important ways [1-3]. While we often think of invasions as a conservation problem stemming from anthropogenic introductions [4,5], biological invasions are much more commonplace than this, including phenomena as diverse as natural range shifts, the spread of novel pathogens, and the growth of tumors. A major question across all these settings is which set of traits determine the ability of a population to invade new space [6,7]. Traits such as: increased growth or reproductive rate, dispersal ability and ability to defend from predation often show large evolutionary shifts across invasion history [1,6,8]. Are such multi-trait shifts driven by selection on multiple traits, or a correlated response by multiple traits to selection on one? Resolving this question is important for both theoretical and practical reasons [9,10]. But despite the importance of this issue, it is not easy to perform the necessary manipulative experiments [9].
Foucaud et al. [11] tackled this issue by performing experimental evolution on source populations of the invasive ladybug Harmonia axyridis. The authors tested if selection on a single trait could generate correlated responses in other life history traits. Specifically, they used experimental evolution to impose divergent selection on female mass, and reproductive timing. After ten generations, they found that selection for weight did not affect almost any other life history trait. However, nine generations of selection for faster reproduction led to correlated phenotypic changes in developmental, reproduction and survival rate of populations, although not always in the direction we might have expected. Despite this correlated response, none of their selected lines were able to fully recapitulate the trait shifts seen in natural invasions of this species. This implies that selection during natural invasions is operating on multiple traits; a finding in agreement with our growing understanding of how selection acts during introduction and invasion [12,13].
Populations undergoing a colonization process may also be subject to a multitude of different selective pressures [14,15]. The authors expanded their work in this direction by testing whether food availability alters the observed correlations between life history traits. The pervasiveness of genotype by environment interactions observed also points to a role for multiple selective pressures in shaping the suite of life-history shifts observed in wild ladybug populations. The work from Foucaud and colleagues [11] adds to a small but growing list of important studies that use experimental evolution to investigate how life-history traits evolve, and how they evolve during invasions in particular.

References

[1] Sakai, A.K., Allendorf, F.W., Holt, J.S. et al. (2001). The population biology of invasive species. Annual review of ecology and systematics, 32(1), 305-332. doi: 10.1146/annurev.ecolsys.32.081501.114037
[2] Hairston Jr, N. G., Ellner, S. P., Geber, M. A., Yoshida, T. and Fox, J. A. (2005). Rapid evolution and the convergence of ecological and evolutionary time. Ecology letters, 8(10), 1114-1127. doi: 10.1111/j.1461-0248.2005.00812.x
[3] Chuang, A. and Peterson, C. R. (2016). Expanding population edges: theories, traits, and trade‐offs. Global change biology, 22(2), 494-512. doi: 10.1111/gcb.13107
[4] Whitney, K. D. and Gabler, C. A. (2008). Rapid evolution in introduced species,‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14(4), 569-580. doi: 10.1111/j.1472-4642.2008.00473.x
[5] Catullo, R. A., Llewelyn, J., Phillips, B. L. and Moritz, C. C. (2019). The Potential for Rapid Evolution under Anthropogenic Climate Change. Current Biology, 29(19), R996-R1007. doi: 10.1016/j.cub.2019.08.028
[6] Suarez, A. V. and Tsutsui, N. D. (2008). The evolutionary consequences of biological invasions. Molecular Ecology, 17(1), 351-360. doi: 10.1111/j.1365-294X.2007.03456.x
[7] Deforet, M., Carmona-Fontaine, C., Korolev, K. S. and Xavier, J. B. (2019). Evolution at the edge of expanding populations. The American Naturalist, 194(3), 291-305. doi: 10.1086/704594
[8] Phillips, B. L., Brown, G. P., and Shine, R. (2010). Life‐history evolution in range‐shifting populations. Ecology, 91(6), 1617-1627. doi: 10.1890/09-0910.1
[9] Colautti, R. I. and Lau, J. A. (2015). Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Molecular ecology, 24(9), 1999-2017. doi: 10.1111/mec.13162
[10] Szűcs, M., Melbourne, B. A., Tuff, T., Weiss‐Lehman, C. and Hufbauer, R. A. (2017). Genetic and demographic founder effects have long‐term fitness consequences for colonising populations. Ecology Letters, 20(4), 436-444. doi: 10.1111/ele.12743
[11] Foucaud, J., Hufbauer, R. A., Ravigné, V., Olazcuaga, L., Loiseau, A., Ausset, A., Wang, S., Zang, L.-S., Lemenager, N., Tayeh, A., Weyna, A., Gneux, P., Bonnet, E., Dreuilhe, V., Poutout, B., Estoup, A. and Facon, B. (2020). How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis. bioRxiv, 849968 ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/849968
[12] Simons, A. M. (2003). Invasive aliens and sampling bias. Ecology Letters, 6(4), 278-280. doi: 10.1046/j.1461-0248.2003.00430.x
[13] Phillips, B. L. and Perkins, T. A. (2019). Spatial sorting as the spatial analogue of natural selection. Theoretical Ecology, 12(2), 155-163. doi: 10.1007/s12080-019-0412-9
[14] Lavergne, S. and Molofsky, J. (2007). Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proceedings of the National Academy of Sciences, 104(10), 3883-3888. doi: 10.1073/pnas.0607324104
[15] Moran, E. V. and Alexander, J. M. (2014). Evolutionary responses to global change: lessons from invasive species. Ecology Letters, 17(5), 637-649. doi: 10.1111/ele.12262

Understanding how species respond to environmental changes is becoming increasingly important in order to predict the future of biodiversity and species distributions under current global warming conditions (Rezende 2020; Bennett et al 2021). Two key factors to take into account in these predictions are the tolerance of organisms to heat stress and subsequently how they adapt to increasingly warmer temperatures. Coupled with this, one important factor that is often overlooked when addressing the evolution of thermal tolerance, is the correlated responses in traits that are important to fitness, such as life histories, behavior and the underlying metabolic processes.

The rate and intensity of the thermal stress are expected to be major factors in shaping the evolution of heat tolerance and correlated responses in other traits. For instance, lower rates of thermal stress are predicted to select for individuals with a slower metabolism (Santos et al 2012), whereas low metabolism is expected to lead to a lower reproductive rate (Dammhahn et al 2018). To quantify the importance of the rate and intensity of thermal stress on the evolutionary response of heat tolerance and correlated response in behavior, Mesas et al (2021) performed experimental evolution in Drosophila subobscura using selective regimes with slow or fast ramping protocols. Whereas both regimes showed increased heat tolerance with similar evolutionary rates, the correlated responses in thermal performance curves for locomotor behavior differed between selection regimes. These findings suggest that thermal rate and intensity may shape the evolution of correlated responses in other traits, urging the need to understand possible correlated responses at relevant levels such as life history and metabolism. 

In the present contribution, Mesas and Castañeda (2022) investigate whether the disparity in thermal performance curves observed in the previous experiment (Mesas et al 2021) could be explained by differences in metabolic energy production and consumption, and how this correlated with the reproductive output (fecundity and viability). Overall, the authors show some evidence for lowered enzyme activity and increased performance in life-history traits, particularly for the slow-ramping selected flies. Specifically, the authors observe a reduction in glucose metabolism and increased viability when evolving under slow ramping stress. Interestingly, both regimes show a general increase in fecundity, suggesting that adaptation to these higher temperatures is not costly (for reproduction) in the ancestral environment. The evidence for a somewhat lower metabolism in the slow-ramping lines suggests the evolution of a slow “pace of life”. The “pace of life” concept tries to bridge variation across several levels namely metabolism, physiology, behavior and life history, with low “pace of life” organisms presenting lower metabolic rates, later reproduction and higher longevity than fast “pace of life” organisms (Dammhahn et al 2018, Tuzun & Stocks 2022).  As the authors state there is not a clear-cut association with the expectations of the pace of life hypothesis since there was evidence for increased reproductive output under both selection intensity regimes. This suggests that, given sufficient trait genetic variance, positively correlated responses may emerge during some stages of thermal evolution. As fecundity estimates in this study were focussed on early life, the possibility of a decrease in the cumulative reproductive output of the selected flies, even under benign conditions, cannot be excluded. This would help explain the apparent paradox of increased fecundity in selected lines. In this context, it would also be interesting to explore the variation in reproductive output at different temperatures, i.e to obtain thermal performance curves for life histories. 

Mesas and Castañeda (2022) raise important questions to pursue in the future and contribute to the growing evidence that, in order to predict the distribution of ectothermic species under current global warming conditions, we need to expand beyond determining the physiological thermal limits of each organism (Parratt et al 2021). Ultimately, integrating metabolic, life-history and behavioral changes during evolution under different thermal stresses within a coherent framework is key to developing better predictions of temperature effects on natural populations.  

References

Bennett, J.M., Sunday, J., Calosi, P. et al. The evolution of critical thermal limits of life on Earth. Nat Commun 12, 1198 (2021). https://doi.org/10.1038/s41467-021-21263-8

Dammhahn, M., Dingemanse, N.J., Niemelä, P.T. et al. Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav Ecol Sociobiol 72, 62 (2018). https://doi.org/10.1007/s00265-018-2473-y

Mesas, A,  Jaramillo, A,  Castañeda, LE.  Experimental evolution on heat tolerance and thermal performance curves under contrasting thermal selection in Drosophila subobscura. J Evol Biol  34, 767– 778 (2021). https://doi.org/10.1111/jeb.13777

Mesas, A, Castañeda, LE Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscura. bioRxiv, 2022.02.03.479001, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.03.479001

Parratt, S.R., Walsh, B.S., Metelmann, S. et al. Temperatures that sterilize males better match global species distributions than lethal temperatures. Nat. Clim. Chang. 11, 481–484 (2021). https://doi.org/10.1038/s41558-021-01047-0

Santos, M, Castañeda, LE, Rezende, EL Keeping pace with climate change: what is wrong with the evolutionary potential of upper thermal limits? Ecology and evolution, 2(11), 2866-2880 (2012). https://doi.org/10.1002/ece3.385

Tüzün, N, Stoks, R. A fast pace-of-life is traded off against a high thermal performance. Proceedings of the Royal Society B, 289(1972), 20212414 (2022). https://doi.org/10.1098/rspb.2021.2414

Rezende, EL, Bozinovic, F, Szilágyi, A, Santos, M. Predicting temperature mortality and selection in natural Drosophila populations. Science, 369(6508), 1242-1245  (2020). https://doi.org/10.1126/science.aba9287

Cytoplasmic incompatibility (CI) is a mating incompatibility that is induced by maternally inherited endosymbionts in many arthropods. These endosymbionts include, most famously, the alpha-proteobacterium Wolbachia pipientis (Yen & Barr 1971; Werren et al. 2008) but also the Bacteroidetes bacterium Cardinium hertigii (Zchori-Fein et al. 2001), a gamma-proteobacterium of the genus Rickettsiella (Rosenwald et al. 2020) and another, as yet undescribed alpha-proteobacterium (Takano et al. 2017). CI manifests as embryonic mortality in crosses between infected males and females that are uninfected or infected with a different strain, whereas embryos develop normally in all other crosses. This phenotype may enable the endosymbionts to spread rapidly within their host population. Exploiting this, CI-inducing Wolbachia are being harnessed to control insect-borne diseases (e.g., O'Neill 2018). Much progress elucidating the genetic basis and developmental mechanism of CI has been made in recent years, but many open questions remain (Shropshire et al. 2020).
Immediately following the discovery and early study of CI in mosquitoes, Laven (1959, 1967) proposed that CI could be an important driver of speciation. Indeed, bi-directional CI can strongly reduce gene flow between two populations due to the elimination of F1 embryos, so that CI can act as a trigger for genetic differentiation in the host (Telschow et al. 2002, 2005). This idea has received much attention, and a potential role for CI in incipient speciation has been demonstrated in several species (e.g., Bordenstein et al. 2001; Jaenike et al. 2006). However, we still don’t know how commonly CI actually triggers speciation, rather than being merely a minor player or secondary phenomenon. The problem is that in addition to CI, postzygotic reproductive isolation can also be caused by host-induced, nuclear incompatibilities. Determining the relative contributions of these two causes of isolation is difficult and has rarely been done.
The study by Cruz et al. (2020) addresses this problem head-on, using a study system of Tetranychus urticae spider mites. These cosmopolitan mites are infected with different strains of Wolbachia. They come in two different colour forms (red and green) that can co-occur sympatrically on the same host plant but exhibit various degrees of reproductive isolation. A complicating factor in spider mites is that they are haplodiploid: unfertilised eggs develop into haploid males and are therefore not affected by any postzygotic incompatibilities, whereas fertilised eggs normally develop into diploid females. In haplodiploids, Wolbachia-induced CI can either kill diploid embryos (as in diplodiploid species), or turn them into haploid males. In their study, Cruz et al. used three different populations (one of the green and two of the red form) and employed a full factorial experiment involving all possible combinations of crosses of Wolbachia infected or uninfected males and females. For each cross, they measured F1 embryonic and juvenile mortality as well as sex ratio, and they also measured F1 fertility and F2 viability. Their results showed that there is strong reduction in hybrid female production caused by Wolbachia-induced CI. However, independent of this and through a different mechanism, there is an even stronger reduction in hybrid production caused by host-associated incompatibilities. In combination with the also observed near-complete sterility of F1 hybrid females and full F2 hybrid breakdown (neither of which is caused by Wolbachia), the results indicate essentially complete reproductive isolation between the green and red forms of T. urticae.
Overall, this is an elegant study with an admirably clean and comprehensive experimental design. It demonstrates that Wolbachia can contribute to reproductive isolation between populations, but that host-induced mechanisms of reproductive isolation predominate in these spider mite populations. Further studies in this exiting system would be useful that also investigate the contribution of pre-zygotic isolation mechanisms such as assortative mating, ascertain whether the results can be generalised to other populations, and – most challengingly – establish the order in which the different mechanisms of reproductive isolation evolved.

References

Bordenstein, S. R., O'Hara, F. P., and Werren, J. H. (2001). Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature, 409(6821), 707-710. doi: https://doi.org/10.1038/35055543
Cruz, M. A., Magalhães, S., Sucena, É., and Zélé, F. (2020) Wolbachia and host intrinsic reproductive barriers contribute additively to post-mating isolation in spider mites. bioRxiv, 2020.06.29.178699, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: https://doi.org/10.1101/2020.06.29.178699
Jaenike, J., Dyer, K. A., Cornish, C., and Minhas, M. S. (2006). Asymmetrical reinforcement and Wolbachia infection in Drosophila. PLoS Biol, 4(10), e325. doi: https://doi.org/10.1371/journal.pbio.0040325
Laven, H. (1959). SPECIATION IN MOSQUITOES Speciation by Cytoplasmic Isolation in the Culex Pipiens-Complex. In Cold Spring Harbor Symposia on Quantitative Biology (Vol. 24, pp. 166-173). Cold Spring Harbor Laboratory Press.
Laven, H. (1967). A possible model for speciation by cytoplasmic isolation in the Culex pipiens complex. Bulletin of the World Health Organization, 37(2), 263-266.
O’Neill S.L. (2018) The Use of Wolbachia by the World Mosquito Program to Interrupt Transmission of Aedes aegypti Transmitted Viruses. In: Hilgenfeld R., Vasudevan S. (eds) Dengue and Zika: Control and Antiviral Treatment Strategies. Advances in Experimental Medicine and Biology, vol 1062. Springer, Singapore. doi: https://doi.org/10.1007/978-981-10-8727-1_24
Rosenwald, L.C., Sitvarin, M.I. and White, J.A. (2020). Endosymbiotic Rickettsiella causes cytoplasmic incompatibility in a spider host. doi: https://doi.org/10.1098/rspb.2020.1107
Shropshire, J. D., Leigh, B., and Bordenstein, S. R. (2020). Symbiont-mediated cytoplasmic incompatibility: what have we learned in 50 years?. Elife, 9, e61989. doi: https://doi.org/10.7554/eLife.61989
Takano et al. (2017). Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle. Proceedings of the National Academy of Sciences, 114(23), 6110-6115. doi: https://doi.org/10.1073/pnas.1618094114
Telschow, A., Hammerstein, P., and Werren, J. H. (2002). The effect of Wolbachia on genetic divergence between populations: models with two-way migration. the american naturalist, 160(S4), S54-S66. doi: https://doi.org/10.1086/342153
Telschow, A., Hammerstein, P., and Werren, J. H. (2005). The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution, 59(8), 1607-1619. doi: https://doi.org/10.1111/j.0014-3820.2005.tb01812.x
Werren, J. H., Baldo, L., and Clark, M. E. (2008). Wolbachia: master manipulators of invertebrate biology. Nature Reviews Microbiology, 6(10), 741-751. doi: https://doi.org/10.1038/nrmicro1969
Yen, J. H., and Barr, A. R. (1971). New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature, 232(5313), 657-658. doi: https://doi.org/10.1038/232657a0
Zchori-Fein, E., Gottlieb, Y., Kelly, S. E., Brown, J. K., Wilson, J. M., Karr, T. L., and Hunter, M. S. (2001). A newly discovered bacterium associated with parthenogenesis and a change in host selection behavior in parasitoid wasps. Proceedings of the National Academy of Sciences, 98(22), 12555-12560. doi: https://doi.org/10.1073/pnas.221467498

The search for physiological markers of health and survival in wild animal populations is attracting a great deal of interest. At present, there is no (and may never be) consensus on such a single, robust marker but of all the proposed physiological markers, telomere length is undoubtedly the most widely studied in the field of evolutionary ecology (Monaghan et al., 2022). 

Broadly speaking, telomeres are non-coding DNA sequences located at the end of chromosomes in eukaryotes, protecting genomic DNA against oxidative stress and various detrimental processes (e.g. DNA end-joining) and thus maintaining genome stability (Blackburn et al., 2015). However, in most somatic cells from the vast majority of the species, telomere sequences are not replicated and telomere length progressively declines with increased age (Remot et al., 2022). This shortening of telomere length upon a critical level is causally linked to cellular senescence and has been invoked as one of the primary causes of the aging process (López-Otín et al., 2023). Studies performed in both captive and wild populations of animals have further demonstrated that short telomeres (or telomere sequences with a fast attrition rate) are to some extent associated with an increased risk of mortality, even if the magnitude of this association largely differs between species and populations (Wilbourn et al., 2018).

The repeated observations of associations between telomere length and mortality risk have called for studies seeking to identify the ecological and biological factors that – beyond chronological age – shape the between-individual variability in telomere length. A wide spectrum of environmental stressors such as the level of exposure to pathogens or the degree of human disturbances has been proposed as possible modulators of telomere dynamics (see Chatelain et al., 2019). However, within species, the relative contribution of various ecological and biological factors on telomere length has been rarely quantified. In that context, the study of Criscuolo and colleagues (2023) constitutes a timely attempt to decipher the relative contribution of environmental and biological factors driving telomere length in nestlings (i.e. when individuals are between 15 and 35 days of age) from a wild population of little owls, Athene noctua.

In addition to chronological age, Criscuolo and colleagues (2023) analysed the effects of two environmental variables (i.e. cohort and habitat quality) as well as three life history traits (i.e. hatching rank, sex and body condition). Among these traits, sex was found to impact nestling’s telomere length with females carrying longer telomeres than males. Traditionally, the among-individuals variability in telomere length during the juvenile period is interpreted as a direct consequence of differences in growth allocation. Fast-growing individuals are typically supposed to undergo more cell divisions and a higher exposure to oxidative stress, which ultimately shortens telomeres (Monaghan & Ozanne, 2018). Whether - despite a slightly female-biased sexual size dimorphism - male little owls display a condensed period of fast growth that could explain their shorter telomere is yet to be determined. Future studies should also explore the consequences of these sex differences in telomere length in terms of mortality risk. In birds, it has been observed that telomere length during early life can predict lifespan (see Heidinger et al., 2012 in zebra finches, Taeniopygia guttata), suggesting that females little owls might live longer than their conspecific males. Yet, adult mortality is generally female-biased in birds (Liker & Székely, 2005) and whether little owls constitute an exception to this rule - possibly mediated by sex-specific telomere dynamics - remains to be explored.   

Quite surprisingly, the present study in little owls did not evidence any clear effect of environmental conditions on nestling’s telomere length, at both temporal and special scales. While a trend for a temporal effect was detected with telomere length being slightly shorter for nestling born the last year of the study (out of 4 years analysed), habitat quality (measured by the proportion of meadow and orchards in the nest environment) had absolutely no impact on nestling telomere length. Recently published studies in wild populations of vertebrates have highlighted the detrimental effects of harsh environmental conditions on telomere length (e.g. Dupoué et al., 2022 in common lizards, Zootoca vivipara), arguing for a key role of telomere dynamics in the emerging field of conservation physiology. While we can recognize the relevance of such an integrative approach, especially in the current context of climate change, the study by Criscuolo and colleagues (2023) reminds us that the relationships between environmental conditions and telomere dynamics are far from straightforward. Depending on the species and its life history, telomere length in early life could indeed capture very different environmental signals.

References

Blackburn, E. H., Epel, E. S., & Lin, J. (2015). Human telomere biology: A contributory and interactive factor in aging, disease risks, and protection. Science, 350(6265), 1193-1198. https://doi.org/10.1126/science.aab3389
 
Chatelain, M., Drobniak, S. M., & Szulkin, M. (2019). The association between stressors and telomeres in non-human vertebrates: A meta-analysis. Ecology Letters, 23, 381-398. https://doi.org/10.1111/ele.13426
 
Criscuolo, F., Fache, I., Scaar, B., Zahn, S. & Bleu, J. (2023). Telomere length vary with sex, hatching rank and year of birth in little owls, Athene noctua. EcoEvoRxiv, ver.4, peer-reviewed and recommended by PCI Evol Biol. https://doi.org/10.32942/X2BS3S
 
Dupoué, A., Blaimont, P., Angelier, F., Ribout, C., Rozen-Rechels, D., Richard, M., & Le Galliard, J. F. (2022). Lizards from warm and declining populations are born with extremely short telomeres. Proceedings of the National Academy of Sciences, 119(33), 2201371119. https://doi.org/10.1073/pnas.2201371119
 
Heidinger, B. J., Blount, J. D., Boner, W., Griffiths, K., Metcalfe, N. B., & Monaghan, P. (2012). Telomere length in early life predicts lifespan. Proceedings of the National Academy of Sciences, 109(5), 1743-1748. https://doi.org/10.1073/pnas.1113306109
 
Liker, A., & Székely, T. (2005). Mortality costs of sexual selection and parental care in natural populations of birds. Evolution, 59(4), 890-897. https://doi.org/10.1111/j.0014-3820.2005.tb01762.x
 
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2023). Hallmarks of aging: An expanding universe. Cell, 186(2), 243-278. https://doi.org/10.1016/j.cell.2022.11.001
 
Monaghan, P., Olsson, M., Richardson, D. S., Verhulst, S., & Rogers, S. M. (2022). Integrating telomere biology into the ecology and evolution of natural populations: Progress and prospects. Molecular Ecology, 31(23), 5909-5916. https://doi.org/10.1111/mec.16768
 
Monaghan, P., & Ozanne, S. E. (2018). Somatic growth and telomere dynamics in vertebrates: Relationships, mechanisms and consequences. Phil. Trans. R. Soc. B, 373(1741), 20160446. https://doi.org/10.1098/rstb.2016.0446
 
Remot, F., Ronget, V., Froy, H., Rey, B., Gaillard, J., Nussey, D. H., & Lemaitre, J. (2022). Decline in telomere length with increasing age across nonhuman vertebrates: A meta‐analysis. Molecular Ecology, 31(23), 5917-5932. https://doi.org/10.1111/mec.16145
 
Wilbourn, R. V., Moatt, J. P., Froy, H., Walling, C. A., Nussey, D. H., & Boonekamp, J. J. (2018). The relationship between telomere length and mortality risk in non-model vertebrate systems: A meta-analysis. Phil. Trans. R. Soc. B, 373(1741), 20160447. https://doi.org/10.1098/rstb.2016.0447