The study of sexual selection goes as far as Darwin himself. Since then, elaborate theories concerning both intra- and inter-sexual sexual have been developed, and elegant experiments have been designed to test this body of theory. It may thus come as a surprise that the community is still debating on the correct way to measure simple components of sexual selection, such as the Bateman gradient (i.e., the covariance between the number of matings and the number of offspring)[1,2], or to quantify complex behaviours such as mate choice (the non-random choice of individuals with particular characters as mates)[3,4] and their consequences.
One difficulty in the study of sexual selection is evaluating the consequences of non-random mating. Indeed, when non-random mating is observed in a population, it is often difficult to establish whether such mating pattern leads to i) sexual selection per se (selection pressures favouring certain phenotypes), and/or ii) the non-random association of parental genes in their offspring or not. These two processes differ. In particular, assortative (and disassortative) mating can shape genetic covariances without leading to changes in gene frequencies in the population. Their distinction matters because these two processes lead to different evolutionary outcomes, which can have large ripple effects in the evolution of sexual behaviours, sexual ornamentation, and speciation.
In his paper, entitled “Multi-model inference of non-random mating from an information theoretic approach” [5], Carvajal-Rodríguez tackled this issue. The author generated a simple model in which the consequences of non-random mating can be inferred from information on the population frequencies before and after mating. The procedure is as follows: from the initial population frequencies of phenotypes (or genotypes) of both sexes, the model generates predictions on the frequencies after mating, assuming that particular mating patterns have occurred. This leads to different predictions for the phenotypic (or genotypic) frequencies after mating. The particular mating pattern leading to the best fit with the real frequencies is then identified via a model selection procedure (performing model averaging to combine different mating patterns is also possible).
This study builds on a framework introduced by Carvajal-Rodríguez’s colleagues [6] and encompasses later methodological developments involving the author himself [7]. Compared to early work, the new method proposed by the author builds on the relationship between mating pattern and information [8] to distinguish among scenarios that would lead to non-random mating due to different underlying processes, using simple model selection criterion such as the AICc.
The great asset of the proposed method is that it can be applied to the study of natural populations in which the study of mate choice and sexual selection is notoriously difficult. In the manuscript, the procedure is tested on a population of marine gastropods (Littorina saxatilis). This allows the reader to grasp how the method can be applied to a real system. In fact, anyone can try out the method thanks to the freely available software InfoMating programmed by the author. One important assumption underlying the current method is that the frequencies of unmated individuals do not change during the mating season. If this is not the case, the reader may refer to another publication of the same author which relaxes this assumption [9]. These papers are both instrumental for empiricists interested in testing sexual selection theory.

References

[1] Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity, 2(3), 349-368. doi: 10.1038/hdy.1948.21
[2] Jones, A. G. (2009). On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution: International Journal of Organic Evolution, 63(7), 1673-1684. doi: 10.1111/j.1558-5646.2009.00664.x
[3] Andersson, M., & Simmons, L. W. (2006). Sexual selection and mate choice. Trends in ecology & evolution, 21(6), 296-302. doi: 10.1016/j.tree.2006.03.015
[4] Kuijper, B., Pen, I., & Weissing, F. J. (2012). A guide to sexual selection theory. Annual Review of Ecology, Evolution, and Systematics, 43, 287-311. doi: 10.1146/annurev-ecolsys-110411-160245
[5] Carvajal-Rodríguez, A. (2019). Multi-model inference of non-random mating from an information theoretic approach. bioRxiv, 305730, ver. 5 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/305730
[6] Rolán‐Alvarez, E., & Caballero, A. (2000). Estimating sexual selection and sexual isolation effects from mating frequencies. Evolution, 54(1), 30-36. doi: 10.1111/j.0014-3820.2000.tb00004.x
[7] Carvajal-Rodríguez, A., & Rolan-Alvarez, E. (2006). JMATING: a software for the analysis of sexual selection and sexual isolation effects from mating frequency data. BMC Evolutionary Biology, 6(1), 40. doi: 10.1186/1471-2148-6-40
[8] Carvajal-Rodríguez, A. (2018). Non-random mating and information theory. Theoretical population biology, 120, 103-113. doi: 10.1016/j.tpb.2018.01.003
[9] Carvajal-Rodríguez, A. (2019). A generalization of the informational view of non-random mating: Models with variable population frequencies. Theoretical population biology, 125, 67-74. doi: 10.1016/j.tpb.2018.12.004

Monnin et al. [1] here studied how Drosophila populations are affected when exposed to a high virulent endosymbiotic wMelPop Wolbachia strain and why virulent vertically transmitting endosymbionts persist in nature. This virulent wMelPop strain has been described to be a blocker of dengue and other arboviral infections in arthropod vector species, such as Aedes aegypti. Whereas it can thus function as a mutualistic symbiont, it here acts as an antagonist along the mutualism-antagonism continuum symbionts operate. The wMelPop strain is not a natural occurring strain in Drosophila melanogaster and thus the start of this experiment can be seen as a novel host-pathogen association. Through experimental evolution of 17 generations, the authors studied how high temperature affects wMelPop Wolbachia virulence and Drosophila melanogaster survival. The authors used Drosophila strains that were selected for late reproduction, given that this should favor evolution to a lower virulence. Assumptions for this hypothesis are not given in the manuscript here, but it can indeed be assumed that energy that is assimilated to symbiont tolerance instead of reproduction may lead to reduced virulence evolution. This has equally been suggested by Reyserhove et al. [2] in a dynamics energy budget model tailored to Daphnia magna virulence evolution upon a viral infection causing White fat Cell disease, reconstructing changing environments through time.
Contrary to their expectations for vertically transmitting symbionts, the authors did not find a reduction in wMelPop Wolbachia virulence during the course of the experimental evolution experiment under high temperature. Important is what this learns for virulence evolution, also for currently horizontal transmitting disease epidemics (such as COVID-19). It mainly reflects that evolution of virulence for new host-pathogen associations is difficult to predict and that it may take multiple generations before optimal levels of virulence are reached [3,4]. These optimal levels of virulence will depend on trade-offs with other life history traits of the symbiont, but also on host demography, host heterogeneity, amongst others [5,6]. Multiple microbial interactions may affect the outcome of virulence evolution [7]. Given that no germ-free individuals were used, it can be expected that other components of the Drosophila microbiome may have played a role in the virulence evolution. In most cases, microbiota have been described as defensive or protective for virulent symbionts [8], but they may also have stimulated the high levels of virulence. Especially, given that upon higher temperatures, Wolbachia growth may have been increased, host metabolic demands increased [9], host immune responses affected and microbial communities changed [10]. This may have resulted in increased competitive interactions to retrieve host resources, sustaining high virulence levels of the symbiont.
A nice asset of this study is that the phenotypic results obtained in the experimental evolution set-up were linked with wMelPop density measurement and octomom copy number quantifications. Octomom is a specific 8-n genes region of the Wolbachia genome responsible for wMelPop virulence, so there is a link between the phenotypic and molecular functions of the involved symbiont. The authors found that density, octomom copy number and virulence were correlated to each other. An important note the authors address in their discussion is that, to exclude the possibility that octomom copy number has an effect on density, and density on virulence, the effect of these variables should be assessed independently of temperature and age. The obtained results are a valuable contribution to the ongoing debate on the relationship between wMelPop octomom copy number, density and virulence.

References

[1] Monnin, D., Kremer, N., Michaud, C., Villa, M., Henri, H., Desouhant, E. and Vavre, F. (2020) Experimental evolution of virulence and associated traits in a Drosophila melanogaster – Wolbachia symbiosis. bioRxiv, 2020.04.26.062265, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: https://doi.org/10.1101/2020.04.26.062265
[2] Reyserhove, L., Samaey, G., Muylaert, K., Coppé, V., Van Colen, W., and Decaestecker, E. (2017). A historical perspective of nutrient change impact on an infectious disease in Daphnia. Ecology, 98(11), 2784-2798. doi: https://doi.org/10.1002/ecy.1994
[3] Ebert, D., and Bull, J. J. (2003). Challenging the trade-off model for the evolution of virulence: is virulence management feasible?. Trends in microbiology, 11(1), 15-20. doi: https://doi.org/10.1016/S0966-842X(02)00003-3
[4] Houwenhuyse, S., Macke, E., Reyserhove, L., Bulteel, L., and Decaestecker, E. (2018). Back to the future in a petri dish: Origin and impact of resurrected microbes in natural populations. Evolutionary Applications, 11(1), 29-41. doi: https://doi.org/10.1111/eva.12538
[5] Day, T., and Gandon, S. (2007). Applying population‐genetic models in theoretical evolutionary epidemiology. Ecology Letters, 10(10), 876-888. doi: https://doi.org/10.1111/j.1461-0248.2007.01091.x
[6] Alizon, S., Hurford, A., Mideo, N., and Van Baalen, M. (2009). Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. Journal of evolutionary biology, 22(2), 245-259. doi: https://doi.org/10.1111/j.1420-9101.2008.01658.x
[7] Alizon, S., de Roode, J. C., and Michalakis, Y. (2013). Multiple infections and the evolution of virulence. Ecology letters, 16(4), 556-567. doi: https://doi.org/10.1111/ele.12076
[8] Decaestecker, E., and King, K. (2019). Red queen dynamics. Reference module in earth systems and environmental sciences, 3, 185-192. doi: https://doi.org/10.1016/B978-0-12-409548-9.10550-0
[9] Kirk, D., Jones, N., Peacock, S., Phillips, J., Molnár, P. K., Krkošek, M., and Luijckx, P. (2018). Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics. PLoS biology, 16(2), e2004608. doi: https://doi.org/10.1371/journal.pbio.2004608
[10] Frankel-Bricker, J., Song, M. J., Benner, M. J., and Schaack, S. (2019). Variation in the microbiota associated with Daphnia magna across genotypes, populations, and temperature. Microbial ecology, 1-12. doi: https://doi.org/10.1007/s00248-019-01412-9

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

Optimal sex ratios have been topic of extensive studies so far. Fisherian 1:1 proportions of males and females are known to be optimal in most (diploid) organisms, but many deviations from this golden rule are observed. These deviations not only attract a lot of attention from evolutionary biologists but also from population ecologists as they eventually determine long-term population growth. Because sex ratios are tightly linked to fitness, they can be under strong selection or plastic in response to changing demographic conditions. Hamilton [1] pointed out that an equality of the sex ratio breaks down when there is local competition for mates. Competition for mates can be considered as a special case of local resource competition. In short, this theory predicts females to adjust their offspring sex ratio conditional on cues indicating the level of local mate competition that their sons will experience. When cues indicate high levels of LMC mothers should invest more resources in the production of daughters to maximise their fitness, while offspring sex ratios should be closer to 50:50 when cues indicate low levels of LMC.
In isolated populations, Macke et al. [2] found sex ratio to evolve fast in response to changes in population sex-structure in the spider mite Tetranychus urticae. Spider mites are becoming top-models in evolutionary biology because of their easy housekeeping, fast generation times and well-studied genome [3]. The species is known to respond fast to changes in relatedness and kin-structure by changing its mating strategy [4], but also dispersal [5]. Sex ratio adjustments are likely mediated by differential investments in egg size, with small eggs possibly experiencing lower chances of fertilization, and thus to develop in haploid males [4].
Alison Duncan and colleagues [6] asked the question whether sex ratios change plastically in response to changes in the local population structure. They additionally questioned whether maternal effects could drive changes in sex-allocation of spider mite mothers. Indeed, theory predicts that if environmental changes are predictable across generations, intergenerational plasticity might be more adaptive than intragenerational plasticity [7]. Especially in spatially structured and highly dynamics populations, female spider mites may experience highly variable demographic conditions from one generation to another. During range expansions, spatial variation in local relatedness and inbreeding are documented to change and to impact eco-evolutionary trajectories as well (e.g. [8]).
Duncan et al. [6] specifically investigate whether the offspring sex ratio of T. urticae females changes in response to 1) the current number of females in the same patch, 2) the number of females in the patches of their mothers and 3) their relatedness to their mate. They surprisingly find the maternal environment to be more important than the actual experienced sex-ratio conditions. These insights thus show the maternal environment to be a reliable predictor of LMC experienced by grand-children. Maternal effects have been found to impact many traits, but this study is the first to convincingly demonstrate maternal effects in sex allocation. It therefore provides an alternative explanation of the apparent fast evolved responses under constant demographic conditions [2], and adds evidence to the importance of non-genetic trait changes for adaptation towards changing demographic and environmental conditions.

References

[1] Hamilton, W. D. (1967). Extraordinary Sex Ratios. Science, 156(3774), 477–488. doi: 10.1126/science.156.3774.477
[2] Macke, E., Magalhães, S., Bach, F., & Olivieri, I. (2011). Experimental evolution of reduced sex ratio adjustment under local mate competition. Science, 334(6059), 1127–1129. doi: 10.1126/science.1212177
[3] Grbić, M., Van Leeuwen, T., Clark, R. M., et al. (2011). The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature, 479(7374), 487–492. doi: 10.1038/nature10640
[4] Macke, E., Magalhães, S., Bach, F., & Olivieri, I. (2012). Sex-ratio adjustment in response to local mate competition is achieved through an alteration of egg size in a haplodiploid spider mite. Proceedings of the Royal Society B: Biological Sciences, 279(1747), 4634–4642. doi: 10.1098/rspb.2012.1598
[5] Bitume, E. V., Bonte, D., Ronce, O., Bach, F., Flaven, E., Olivieri, I., & Nieberding, C. M. (2013). Density and genetic relatedness increase dispersal distance in a subsocial organism. Ecology Letters, 16(4), 430–437. doi: 10.1111/ele.12057
[6] Duncan, A., Marinosci, C., Devaux, C., Lefèvre, S., Magalhães, S., Griffin, J., Valente, A., Ronce, O., Olivieri, I. (2018). Transgenerational cues about local mate competition affect offspring sex ratios in the spider mite Tetranychus urticae. BioRxiv, 240127, ver. 3. doi: 10.1101/240127
[7] Petegem, K. V., Moerman, F., Dahirel, M., Fronhofer, E. A., Vandegehuchte, M. L., Leeuwen, T. V., Wybouw, N., Stoks, R., Bonte, D. (2018). Kin competition accelerates experimental range expansion in an arthropod herbivore. Ecology Letters, 21(2), 225–234. doi: 10.1111/ele.12887
[8] Marshall, D. J., & Uller, T. (2007). When is a maternal effect adaptive? Oikos, 116(12), 1957–1963. doi: 10.1111/j.2007.0030-1299.16203.x

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