- Département de Biologie & Institut de Biologie Intégrative et des Systèmes, Université Laval, Québec, Canada
- Adaptation, Behavior & Social Evolution, Expression Studies, Genotype-Phenotype, Life History, Phenotypic Plasticity
Dynamics of sex-biased gene expression over development in the stick insect <i>Timema californicum</i>
Sex-biased gene expression in an hemimetabolous insect: pattern during development, extent, functions involved, rate of sequence evolution, and comparison with an holometabolous insectRecommended by Nadia Aubin-Horth based on reviews by 2 anonymous reviewers
An individual’s sexual phenotype is determined during development. Understanding which pathways are activated or repressed during the developmental stages leading to a sexually mature individual, for example by studying gene expression and how its level is biased between sexes, allows us to understand the functional aspects of dimorphic phenotypes between the sexes.
Several studies have quantified the differences in transcription between the sexes in mature individuals, showing the extent of this sex-bias and which functions are affected. There is, however, less data available on what occurs during the different phases of development leading to this phenotype, especially in species with specific developmental strategies, such as hemimetabolous insects. While many well-studied insects such as the honey bee, drosophila, and butterflies, exhibit an holometabolous development ("holo" meaning "complete" in reference to their drastic metamorphosis from the juvenile to the adult stage), hemimetabolous insects have juvenile stages that look similar to the adult stage (the hemi prefix meaning "half", referring to the more tissue-specific changes during development), as seen in crickets, cockroaches, and stick insects. Learning more about what happens during development in terms of the identity of genes that are sex-biased (are they the same genes at different developmental stages? What are their function? Do they exhibit specific sequence evolution rates? Is one sex over-represented in the sex-biased genes?) and their quantity over developmental time (gradual or abrupt increase in number, if any?) would allow us to better understand the evolution of sexual dimorphism at the gene expression level and how it relates to dimorphism at the organismic level.
Djordjevic et al (2021) studied the transcriptome during development in an hemimetabolous stick insect, to improve our knowledge of this type of development, where the organismic phenotype is already mostly present in the early life stages. To do this, they quantified whole-genome gene expression levels in whole insects, using RNA-seq at three different developmental stages. One of the interesting results presented by Djordjevic and colleagues is that the increase in the number of genes that were sex-biased in expression is gradual over the three stages of development studied and it is mostly the same genes that stay sex-biased over time, reflecting the gradual change in phenotypes between hatchlings, juveniles and adults. Furthermore, male-biased genes had faster sequence divergence rates than unbiased genes and that female-biased genes.
This new information of sex-bias in gene expression in an hemimetabolous insect allowed the authors to do a comparison of sex-biased genes with what has been found in a well-studied holometabolous insect, Drosophila. The gene expression patterns showed that four times more genes were sex-biased in expression in that species than in stick insects. Furthermore, the increase in the number of sex-biased genes during development was quite abrupt and clearly distinct in the adult stage, a pattern that was not seen in stick insects. As pointed out by the authors, this pattern of a "burst" of sex-biased genes at maturity is more common than the gradual increase seen in stick insects.
With this study, we now know more about the evolution of sex-biased gene expression in an hemimetabolous insect and how it relates to their phenotypic dimorphism. Clearly, the next step will be to sample more hemimetabolous species at different life stages, to see how this pattern is widespread or not in this mode of development in insects.
Djordjevic J, Dumas Z, Robinson-Rechavi M, Schwander T, Parker DJ (2021) Dynamics of sex-biased gene expression during development in the stick insect Timema californicum. bioRxiv, 2021.01.23.427895, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.01.23.427895
Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig
Assessing the role of host-symbiont interactions in maternal care behaviourRecommended by Trine Bilde based on reviews by Nadia Aubin-Horth, Gabrielle Davidson and 1 anonymous reviewer
The role of microbial symbionts in governing social traits of their hosts is an exciting and developing research area. Just like symbionts influence host reproductive behaviour and can cause mating incompatibilities to promote symbiont transmission through host populations (Engelstadter and Hurst 2009; Correa and Ballard 2016; Johnson and Foster 2018) (see also discussion on conflict resolution in Johnsen and Foster 2018), microbial symbionts could enhance transmission by promoting the social behaviour of their hosts (Ezenwa et al. 2012; Lewin-Epstein et al. 2017; Gurevich et al. 2020). Here I apply the term ‘symbiosis’ in the broad sense, following De Bary 1879 as “the living together of two differently named organisms“ independent of effects on the organisms involved (De Bary 1879), i.e. the biological interaction between the host and its symbionts may include mutualism, parasitism and commensalism.
So far, we have relative few studies that explore the role of symbionts in promoting social behaviours such as parental care. Clearly, disentangling cause and effect when assessing the functional significance of symbiotic relationships in general is extremely challenging, and perhaps even more caution is needed when assessing the role of symbionts in the evolution of parental care, given the high fitness benefits to the offspring of receiving care. An interesting study on the symbiotic relationship between termites and their eukaryotic gut symbionts proposes a role of gut flagellates in the origin of subsocial behaviour (extended offspring care) in the termites through proctodeal trophallaxis (i.e. anus-to-mouth feeding), driven by mutualistic beneficial interactions (Nalepa 2020). Van Meyel et al. (2021) hypothesized a role of gut symbionts in promoting maternal care behaviour in the European earwig, and set out to test this idea in a carefully executed experimental study. They used a broad-spectrum antibiotic treatment to alter gut microbiota in mothers and examined its effect on maternal care provisioning. While the antibiotic treatment altered the gut microbiome, no effect on pre- or post-hatching maternal care was detected. The authors also investigated a broad range of physiological and reproductive traits measured over a major part of a female’s lifetime, and detected no effect of microbiome alteration on these traits. The study therefore does not provide evidence for a direct role of the gut microbiome in shaping offspring care in this population of European earwigs.
Within populations, earwigs show inter-individual variation in the expression of maternal care (Meunier et al. 2012; Ratz et al. 2016), and there is evidence that genetic and environmental factors contribute to this this variation (Meunier and Kolliker 2012; Kramer et al. 2017). The study by Van Meyel et al. (2021) is the first to analyse microbiome composition of the European earwig, and they study host-symbiont associations in a single population. A next step could be to explore among population variation in the gut microbiome, to achieve a better understanding on host-microbiome variation and dynamics in wild populations. Depending on the nature of host-symbiont associations across populations, new perspectives on their functional significance may arise (Hird 2017; Johnson and Foster 2018). It is therefore too early to conclusively confirm or reject the role of microbial symbionts in the expression of parental care in this system.
Correa, C. C., and Ballard, J. W. O. (2016). Wolbachia associations with insects: winning or losing against a master manipulator. Frontiers in Ecology and Evolution, 3, 153. doi: https://doi.org/10.3389/fevo.2015.00153
De Bary, A. (1879). Die Erscheinung der Symbiose. Verlag von Karl J. Trubner, Strassburg.
Engelstädter, J., and Hurst, G. D. (2009). The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology, Evolution, and Systematics, 40, 127-149. doi: https://doi.org/10.1146/annurev.ecolsys.110308.120206
Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M., and Xavier, J. B. (2012). Animal behavior and the microbiome. Science, 338(6104), 198-199. doi: https://doi.org/10.1126/science.1227412
Gurevich, Y., Lewin-Epstein, O., and Hadany, L. (2020). The evolution of paternal care: a role for microbes?. Philosophical Transactions of the Royal Society B, 375(1808), 20190599. doi: https://doi.org/10.1098/rstb.2019.0599
Hird, S. M. (2017). Evolutionary biology needs wild microbiomes. Frontiers in microbiology, 8, 725. doi: https://doi.org/10.3389/fmicb.2017.00725
Johnson, K. V. A., and Foster, K. R. (2018). Why does the microbiome affect behaviour?. Nature reviews microbiology, 16(10), 647-655. doi: https://doi.org/10.1038/s41579-018-0014-3
Kramer et al. (2017). When earwig mothers do not care to share: parent–offspring competition and the evolution of family life. Functional Ecology, 31(11), 2098-2107. doi: https://doi.org/10.1111/1365-2435.12915
Lewin-Epstein, O., Aharonov, R., and Hadany, L. (2017). Microbes can help explain the evolution of host altruism. Nature communications, 8(1), 1-7. doi: https://doi.org/10.1038/ncomms14040
Meunier, J., and Kölliker, M. (2012). Parental antagonism and parent–offspring co-adaptation interact to shape family life. Proceedings of the Royal Society B: Biological Sciences, 279(1744), 3981-3988. doi: https://doi.org/10.1098/rspb.2012.1416
Meunier, J., Wong, J. W., Gómez, Y., Kuttler, S., Röllin, L., Stucki, D., and Kölliker, M. (2012). One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig. Evolutionary Ecology, 26(3), 669-682. doi: https://doi.org/10.1007/s10682-011-9510-x
Nalepa, C. A. (2020). Origin of mutualism between termites and flagellated gut protists: transition from horizontal to vertical transmission. Frontiers in Ecology and Evolution, 8, 14. doi: https://doi.org/10.3389/fevo.2020.00014
Ratz, T., Kramer, J., Veuille, M., and Meunier, J. (2016). The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care. Oecologia, 182(2), 443-452. doi: https://doi.org/10.1007/s00442-016-3685-3
Van Meyel, S., Devers, S., Dupont, S., Dedeine, F. and Meunier, J. (2021) Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig. bioRxiv, 2020.10.08.331363. ver. 5 peer-reviewed and recommended by PCI Evol Biol. https://doi.org/10.1101/2020.10.08.331363
Natural selection on plasticity of thermal traits in a highly seasonal environment
Is thermal plasticity itself shaped by natural selection? An assessment with desert frogsRecommended by Wolf Blanckenhorn based on reviews by Nadia Aubin-Horth, Wolf Blanckenhorn and Dries Bonte
It is well known that climatic factors – most notably temperature, season length, insolation and humidity – shape the thermal niche of organisms on earth through the action of natural selection. But how is this achieved precisely? Much of thermal tolerance is actually mediated by phenotypic plasticity (as opposed to genetic adaptation). A prominent expectation is that environments with greater (daily and/or annual) thermal variability select for greater plasticity, i.e. better acclimation capacity. Thus, plasticity might be selected per se.
A Chilean group around Leonardo Bacigalupe assessed natural selection in the wild in one marginal (and extreme) population of the four-eyed frog Pleurodema thaul (Anura: Leptodactylidae) in an isolated oasis in the Atacama Desert, permitting estimation of mortality without much potential of confounding it with migration . Several thermal traits were considered: CTmax – the critical maximal temperature; CTmin – the critical minimum temperature; Tpref – preferred temperature; Q10 – thermal sensitivity of metabolism; and body mass. Animals were captured in the wild and subsequently assessed for thermal traits in the laboratory at two acclimation temperatures (10° & 20°C), defining the plasticity in all traits as the difference between the traits at the two acclimation temperatures. Thereafter the animals were released again in their natural habitat and their survival was monitored over the subsequent 1.5 years, covering two breeding seasons, to estimate viability selection in the wild. The authors found and conclude that, aside from larger body size increasing survival (an unsurprising result), plasticity does not seem to be systematically selected directly, while some of the individual traits show weak signs of selection.
Despite limited sample size (ca. 80 frogs) investigated in only one marginal but very seasonal population, this study is interesting because selection on plasticity in physiological thermal traits, as opposed to selection on the thermal traits themselves, is rarely investigated. The study thus also addressed the old but important question of whether plasticity (i.e. CTmax-CTmin) is a trait by itself or an epiphenomenon defined by the actual traits (CTmax and CTmin) [2-5]. Given negative results, the main question could not be ultimately solved here, so more similar studies should be performed.
 Bacigalupe LD, Gaitan-Espitia, JD, Barria AM, Gonzalez-Mendez A, Ruiz-Aravena M, Trinder M & Sinervo B. 2018. Natural selection on plasticity of thermal traits in a highly seasonal environment. bioRxiv 191825, ver. 5 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/191825
 Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annual Review in Ecology and Systematics 24: 35–68. doi: 10.1146/annurev.es.24.110193.000343
 Scheiner SM. 1993. Plasticity as a selectable trait: Reply to Via. The American Naturalist. 142: 371–373. doi: 10.1086/285544
 Via S. 1993. Adaptive phenotypic plasticity - Target or by-product of selection in a variable environment? The American Naturalist. 142: 352–365. doi: 10.1086/285542
 Via S. 1993. Regulatory genes and reaction norms. The American Naturalist. 142: 374–378. doi: 10.1086/285542