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18 Nov 2022
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Fitness costs and benefits in response to artificial artesunate selection in Plasmodium

The importance of understanding fitness costs associated with drug resistance throughout the life cycle of malaria parasites

Recommended by based on reviews by Sarah Reece and Marianna Szucs

Antimalarial resistance is a major hurdle to malaria eradication efforts. The spread of drug resistance follows basic evolutionary principles, with competitive interactions between resistant and susceptible malaria strains being central to the fitness of resistant parasites. These competitive interactions can be used to design resistance management strategies, whereby a fitness cost of resistant parasites can be exploited through maintaining competitive suppression of the more fit drug-susceptible parasites. This can potentially be achieved using lower drug dosages or lower frequency of drug treatments. This approach has been demonstrated to work empirically in a rodent malaria model [1,2] and has been demonstrated to have clinical success in cancer treatments [3]. However, these resistance management approaches assume a fitness cost of the resistant pathogen, and, in the case of malaria parasites in general, and for artemisinin resistant parasites in particular, there is limited information on the presence of such fitness cost. The best suggestive evidence for the presence of fitness costs comes from the discontinuation of the use of the drug, which, in the case of chloroquine, was followed by a gradual drop in resistance frequency over the following decade [see e.g. 4,5]. However, with artemisinin derivative drugs still in use, alternative ways to study the presence of fitness costs need to be undertaken. 
There are several good in vitro studies demonstrating artemisinin resistant parasites being competitively suppressed by wildtype parasites [see e.g. 6–9], however, these have the limitation that they will only be able to detect the fitness cost during the blood stage of the infection and in an artificial environment. So far, there have not been animal models that have thoroughly studied the presence of resistance fitness costs for artemisinin resistant parasites. Moreover, in these types of studies, the focus is mostly on the fitness cost as detected in the vertebrate host. However, malaria parasites spent a significant portion of their life cycle in the mosquito host, where fitness costs could also be expressed. Overall, it is the fitness over the entire life cycle of the parasite that would determine if and to what extent a reduction in resistance frequency would be observed when the use of a drug is stopped. 
Here, Villa and colleagues present a study to quantify such fitness cost of artesunate-resistant parasites, not only in a vertebrate host, but also in the mosquito vector [10]. They used the underutilized model system of avian malaria species Plasmodium relictum in canaries. Villa and colleagues selected for several different resistance strains, which had a similar delayed clearance phenotype as observed in the field. Interestingly, they did not find evidence of a fitness cost in the vertebrate host. In fact, the resistant strains reached greater parasitaemia than the susceptible strains. From this set of experiments it is unclear whether this is an anomaly or a relevant result. Future work should establish this, though fitness benefits associated with drug resistance have been seen before in Leishmania parasites [11]. An important caveat to the present study is that the parasites were grown in the absence of competition and it is feasible that a cost is not detected when growing by themselves, but would become apparent when in competition. However, these types of experiments are technologically more challenging to perform as it would require an accurate quantification methodology able to distinguish based on one SNP. This problem has been circumvented by either using relative peak height in sanger sequencing [12], or via the likely more accurate route of pyrosequencing [7–9], though these methodologies only give relative frequencies rather than absolute densities. 
 
The most interesting observation in the study by Villa et al is that the authors detected a fitness cost being played out in the mosquito vector, where the resistant strains had a decreased infectivity compared to the susceptible strain. This finding is important because 1) it demonstrates that the whole life cycle needs to be taken into account when understanding fitness costs, 2) resistance management strategies that are based on treatment within the vertebrate host may not have the intended effect if the cost does not play out in this host, and 3) it opens new research avenues to explore the possibility of exploiting fitness costs in mosquito vector. Future research should focus on incorporating these assays on fitness costs in mosquitoes, particularly for P. falciparum parasites. Additionally, it would be interesting to expand this work in a competitive environment, both in the vertebrate host as in the mosquito host. Finally, it would be important to establish the generalizability of such fitness cost in mosquitoes. If it is a significant factor, mathematical models could incorporate this effect in predictions on the spread of resistance.

References

[1] Huijben S, Bell AS, Sim DG, Tomasello D, Mideo N, Day T, et al. 2013. Aggressive chemotherapy and the selection of drug resistant pathogens. PLoS Pathog. 9(9): e1003578. https://doi.org/10.1371/journal.ppat.1003578
 
[2] Huijben S, Nelson WA, Wargo AR, Sim DG, Drew DR, Read AF. 2010. Chemotherapy, within-host ecology and the fitness of drug-resistant malaria parasites. Evolution (N Y). 64(10): 2952-68. https://doi.org/10.1111/j.1558-5646.2010.01068.x
 
[3] Zhang J, Cunningham JJ, Brown JS, Gatenby RA. 2017. Integrating evolutionary dynamics into treatment of metastatic castrate-resistant prostate cancer. Nat Commun. 8(1). https://doi.org/10.1038/s41467-017-01968-5
 
[4] Laufer MK, Takala-Harrison S, Dzinjalamala FK, Stine OC, Taylor TE, Plowe C v. 2010. Return of chloroquine-susceptible falciparum malaria in Malawi was a reexpansion of diverse susceptible parasites. J Infect Dis. 202(5): 801-808. https://doi.org/10.1086/655659 

[5] Mharakurwa S, Matsena-Zingoni Z, Mudare N, Matimba C, Gara TX, Makuwaza A, et al. 2021. Steep rebound of chloroquine-sensitive Plasmodium falciparum in Zimbabwe. J Infect Dis. 223(2): 306-9. https://doi.org/10.1093/infdis/jiaa368
 
[6] Tirrell AR, Vendrely KM, Checkley LA, Davis SZ, McDew-White M, Cheeseman IH, et al. 2019. Pairwise growth competitions identify relative fitness relationships among artemisinin resistant Plasmodium falciparum field isolates. Malar J. 18: 295. https://doi.org/10.1186/s12936-019-2934-4
 
[7] Hott A, Tucker MS, Casandra D, Sparks K, Kyle DE. 2015. Fitness of artemisinin-resistant Plasmodium falciparum in vitro. J Antimicrob Chemother. 70(10): 2787-2796. https://doi.org/10.1093/jac/dkv199
 
[8] Straimer J, Gnädig NF, Stokes BH, Ehrenberger M, Crane AA, Fidock DA. 2017. Plasmodium falciparum K13 mutations differentially impact ozonide susceptibility and parasite fitness in vitro. mBio. 8(2): e00172-17. https://doi.org/10.1128/mBio.00172-17
 
[9] Nair S, Li X, Arya GA, McDew-White M, Ferrari M, Nosten F, et al. 2018. Fitness costs and the rapid spread of kelch13-C580Y substitutions conferring artemisinin resistance. Antimicrob Agents Chemother. 62(9). https://doi.org/10.1128/AAC.00605-18
 
[10] Villa M, Berthomieu A, Rivero A. Fitness costs and benefits in response to artificial artesunate selection in Plasmodium. 2022. bioRxiv, 20220128478164, ver 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.01.28.478164
 
[11] Vanaerschot M, Decuypere S, Berg M, Roy S, Dujardin JC. 2013. Drug-resistant microorganisms with a higher fitness--can medicines boost pathogens? Crit Rev Microbiol. 39(4): 384-394. https://doi.org/10.3109/1040841X.2012.716818
 
[12] Hassett MR, Roepe PD. In vitro growth competition experiments that suggest consequences of the substandard artemisinin epidemic that may be accelerating drug resistance in P. falciparum malaria. 2021. PLoS One. 16(3): e0248057. https://doi.org/10.1371/journal.pone.0248057

Fitness costs and benefits in response to artificial artesunate selection in PlasmodiumVilla M, Berthomieu A, Rivero A<p style="text-align: justify;">Drug resistance is a major issue in the control of malaria. Mutations linked to drug resistance often target key metabolic pathways and are therefore expected to be associated with biological costs. The spread of dr...Evolutionary Applications, Life HistorySilvie Huijben2022-01-31 13:01:16 View
16 Nov 2022
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Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

Tinder in mice: A match made with the sense of smell

Recommended by ORCID_LOGO based on reviews by Angeles de Cara, Ludovic Claude Maisonneuve and 1 anonymous reviewer

Differentiation-based genome scans lie at the core of speciation and adaptation genomics research. Dating back to Lewontin & Krakauer (1973), they have become very popular with the advent of genomics to identify genome regions of enhanced differentiation relative to neutral expectations. These regions may represent genetic barriers between divergent lineages and are key for studying reproductive isolation. However, genome scan methods can generate a high rate of false positives, primarily if the neutral population structure is not accounted for (Bierne et al. 2013). Moreover, interpreting genome scans can be challenging in the context of secondary contacts between diverging lineages (Bierne et al. 2011), because the coupling between different components of reproductive isolation (local adaptation, intrinsic incompatibilities, mating preferences, etc.) can occur readily, thus preventing the causes of differentiation from being determined.

Smadja and collaborators (2022) applied a sophisticated genome scan for trait association (BAYPASS, Gautier 2015) to underlie the genetic basis of a polygenetic behaviour: assortative mating in hybridizing mice. My interest in this neat study mainly relies on two reasons. First, the authors used an ingenious geographical setting (replicate pairs of “Choosy” versus “Non-Choosy” populations) with multi-way comparisons to narrow down the list of candidate regions resulting from BAYPASS. The latter corrects for population structure, handles cost-effective pool-seq data and allows for gene-based analyses that aggregate SNP signals within a gene. These features reinforce the set of outlier genes detected; however, not all are expected to be associated with mating preference. 

The second reason why this study is valuable to me is that Smadja et al. (2022) complemented the population genomic approach with functional predictions to validate the genetic signal. In line with previous behavioural and chemical assays on the proximal mechanisms of mating preferences, they identified multiple olfactory and vomeronasal receptor genes as highly significant candidates. Therefore, combining genomic signals with functional analyses is a clever way to provide insights into the causes of reproductive isolation, especially when multiple barriers are involved. This is typically true for reinforcement (Butlin & Smadja 2018), suspected to occur in these mice because, in that case, assortative mating (a prezygotic barrier) evolves in response to the cost of hybridization (for example, due to hybrid inviability). 

As advocated by the authors, their study paves the way for future work addressing the genetic basis of reinforcement, a trait of major evolutionary importance for which we lack empirical data. They also make a compelling case using complementary approaches that olfactory and vomeronasal receptors have a central role in mammal speciation.


References:

Bierne N, Welch J, Loire E, Bonhomme F, David P (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol Ecol 20: 2044–2072. https://doi.org/10.1111/j.1365-294X.2011.05080.x

Bierne N, Roze D, Welch JJ (2013) Pervasive selection or is it…? why are FST outliers sometimes so frequent? Mol Ecol 22: 2061–2064. https://doi.org/10.1111/mec.12241 

Butlin RK, Smadja CM (2018) Coupling, Reinforcement, and Speciation. Am Nat 191:155–172. https://doi.org/10.1086/695136 

Gautier M (2015) Genome-Wide Scan for Adaptive Divergence and Association with Population-Specific Covariates. Genetics 201:1555–1579. https://doi.org/10.1534/genetics.115.181453 

Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of selective neutrality of polymorphisms. Genetics 74: 175–195. https://doi.org/10.1093/genetics/74.1.175 

Smadja CM, Loire E, Caminade P, Severac D, Gautier M, Ganem G (2022) Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice. bioRxiv, 2022.07.21.500634, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.07.21.500634

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in miceCarole M. Smadja, Etienne Loire, Pierre Caminade, Dany Severac, Mathieu Gautier, Guila Ganem<p>Deciphering the genetic bases of behavioural traits is essential to understanding how they evolve and contribute to adaptation and biological diversification, but it remains a substantial challenge, especially for behavioural traits with polyge...Adaptation, Behavior & Social Evolution, Genotype-Phenotype, SpeciationChristelle Fraïsse2022-07-25 11:54:52 View
02 Nov 2022
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Evolution of immune genes in island birds: reduction in population sizes can explain island syndrome

Demographic effects may affect adaptation to islands

Recommended by based on reviews by Steven Fiddaman and 3 anonymous reviewers

The unique challenges associated with living on an island often result in organisms displaying a specific suite of traits commonly referred to as “island syndrome” (Adler and Levins, 1994; Burns, 2019; Baeckens and Van Damme, 2020). Large phenotypic shifts such as changes in size (e.g. shifts to gigantism or dwarfism, Lomolino, 2005) or coloration (Doutrelant et al., 2016) abound in the literature. However, less obvious phenotypes may also play a key role in adaptation to islands.

One such trait, reduced immune function, has important implications for the future of island populations in the face of anthropogenic-induced changes. Due to lower parasite pressure caused by a less diverse and less virulent parasite population, island hosts may show a decrease in immune defenses (Beadell et al., 2006; Pérez‐Rodríguez et al., 2013). However, this hypothesis has been challenged, as many studies have found ambiguous or conflicting results (Matson, 2006; Illera et al., 2015).

While most previous work has examined various immunological parameters (e.g., antibody concentrations), here, Barthe et al. (2022) take the novel approach of examining molecular signatures of immune genes. Using comparative genomic data from 34 different species of birds the authors examine the ratio of synonymous substitutions (i.e., not changing an amino acid) to non-synonymous substitutions (i.e., changing an amino acid) in innate and acquired immune genes (Pn/Ps ratio). Because population sizes on islands are lower which will affect molecular evolution, they compare these results to data from 97 control genes.  Assuming relaxed selection on islands predicts that the difference between the Pn/Ps ratio of immune genes and of control genes (ΔPn/Ps) is greater in island species compared to mainland ones.

As with previous work the authors found that the results differ depending on the category of immune genes. Both forms of innate defense: beta-defensins and Toll-like receptors did not show higher ΔPn/Ps for island populations. As these genes still have a higher Pn/Ps than control genes, the authors argue these results are in line with these genes being under purifying selection but lacking an “island effect”. Instead, the authors argue that demographic effects (i.e., reductions in Ne) may lead to the decreased immunity documented in other studies. In contrast, there was a reduction in Pn/Ps in MHC II genes, known to be under balancing selection. This reduction was stronger in island species and thus the authors argue that this is the only class of genes where a role for relaxed selection can be invoked. 

Together these results demonstrate that the changes in immunity experienced by island species are complex and that different categories of immune genes can experience different selective pressures. By including control genes in their study, they particularly highlight the importance of accounting for shifts in Ne when examining patterns of island species evolution. Hopefully, this kind of framework will be applied to other taxa to determine if these results are widespread or more specific to birds. 

References

Adler GH, Levins R (1994) The Island Syndrome in Rodent Populations. The Quarterly Review of Biology, 69, 473–490. https://doi.org/10.1086/418744

Baeckens S, Van Damme R (2020) The island syndrome. Current Biology, 30, R338–R339. https://doi.org/10.1016/j.cub.2020.03.029

Barthe M, Doutrelant C, Covas R, Melo M, Illera JC, Tilak M-K, Colombier C, Leroy T, Loiseau C, Nabholz B (2022) Evolution of immune genes in island birds: reduction in population sizes can explain island syndrome. bioRxiv, 2021.11.21.469450, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.11.21.469450

Beadell JS, Ishtiaq F, Covas R, Melo M, Warren BH, Atkinson CT, Bensch S, Graves GR, Jhala YV, Peirce MA, Rahmani AR, Fonseca DM, Fleischer RC (2006) Global phylogeographic limits of Hawaii’s avian malaria. Proceedings of the Royal Society B: Biological Sciences, 273, 2935–2944. https://doi.org/10.1098/rspb.2006.3671

Burns KC (2019) Evolution in Isolation: The Search for an Island Syndrome in Plants. Cambridge University Press, Cambridge. https://doi.org/10.1017/9781108379953

Doutrelant C, Paquet M, Renoult JP, Grégoire A, Crochet P-A, Covas R (2016) Worldwide patterns of bird colouration on islands. Ecology Letters, 19, 537–545. https://doi.org/10.1111/ele.12588

Illera JC, Fernández-Álvarez Á, Hernández-Flores CN, Foronda P (2015) Unforeseen biogeographical patterns in a multiple parasite system in Macaronesia. Journal of Biogeography, 42, 1858–1870. https://doi.org/10.1111/jbi.12548

Lomolino MV (2005) Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography, 32, 1683–1699. https://doi.org/10.1111/j.1365-2699.2005.01314.x

Matson KD (2006) Are there differences in immune function between continental and insular birds? Proceedings of the Royal Society B: Biological Sciences, 273, 2267–2274. https://doi.org/10.1098/rspb.2006.3590

Pérez-Rodríguez A, Ramírez Á, Richardson DS, Pérez-Tris J (2013) Evolution of parasite island syndromes without long-term host population isolation: parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography, 22, 1272–1281. https://doi.org/10.1111/geb.12084

Evolution of immune genes in island birds: reduction in population sizes can explain island syndromeMathilde BARTHE, Claire DOUTRELANT, Rita COVAS, Martim MELO, Juan Carlos ILLERA, Marie-Ka TILAK, Constance COLOMBIER, Thibault LEROY , Claire LOISEAU , Benoit NABHOLZ<p style="text-align: justify;">Shared ecological conditions encountered by species that colonize islands often lead to the evolution of convergent phenotypes, commonly referred to as “island syndrome”. Reduced immune functions have been previousl...Adaptation, Molecular Evolution, Population Genetics / GenomicsEmma Berdan2021-11-28 11:01:31 View
31 Oct 2022
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Genotypic sex shapes maternal care in the African Pygmy mouse, Mus minutoides

Effect of sex chromosomes on mammalian behaviour: a case study in pygmy mice

Recommended by and ORCID_LOGO based on reviews by Marion Anne-Lise Picard, Caroline Hu and 1 anonymous reviewer

In mammals, it is well documented that sexual dimorphism and in particular sex differences in behaviour are fine-tuned by gonadal hormonal profiles. For example, in lemurs, where female social dominance is common, the level of testosterone in females is unusually high compared to that of other primate females (Petty and Drea 2015). 

Recent studies however suggest that gonadal hormones might not be the only biological factor involved in establishing sexual dimorphism, sex chromosomes might also play a role. The four core genotype (FCG) model and other similar systems allowing to decouple phenotypic and genotypic sex in mice have provided very convincing evidence of such a role (Gatewood et al. 2006; Arnold and Chen 2009; Arnold 2020a, 2020b). This however is a new field of research and the role of sex chromosomes in establishing sexually dimorphic behaviours has not been studied very much yet. Moreover, the FCG model has some limits. Sry, the male determinant gene on the mammalian Y chromosome might be involved in some sex differences in neuroanatomy, but Sry is always associated with maleness in the FCG model, and this potential role of Sry cannot be studied using this system.

Heitzmann et al. have used a natural system to approach these questions. They worked on the African Pygmy mouse, Mus minutoides, in which a modified X chromosome called X* can feminize X*Y individuals, which offers a great opportunity for elegant experiments on the effects of sex chromosomes versus hormones on behaviour. They focused on maternal care and compared pup retrieval, nest quality, and mother-pup interactions in XX, X*X and X*Y females. They found that X*Y females are significantly better at retrieving pups than other females. They are also much more aggressive towards the fathers than other females, preventing paternal care. They build nests of poorer quality but have similar interactions with pups compared to other females. Importantly, no significant differences were found between XX and X*X females for these traits, which points to an effect of the Y chromosome in explaining the differences between X*Y and other females (XX, X*X). Also, another work from the same group showed similar gonadal hormone levels in all the females (Veyrunes et al. 2022). 

Heitzmann et al. made a number of predictions based on what is known about the neuroanatomy of rodents which might explain such behaviours. Using cytology, they looked for differences in neuron numbers in the hypothalamus involved in the oxytocin, vasopressin and dopaminergic pathways in XX, X*X and X*Y females, but could not find any significant effects. However, this part of their work relied on very small sample sizes and they used virgin females instead of mothers for ethical reasons, which greatly limited the analysis. 

Interestingly, X*Y females have a higher reproductive performance than XX and X*X ones, which compensate for the cost of producing unviable YY embryos and certainly contribute to maintaining a high frequency of X* in many African pygmy mice populations (Saunders et al. 2014, 2022). X*Y females are probably solitary mothers contrary to other females, and Heitzmann et al. have uncovered a divergent female strategy in this species. Their work points out the role of sex chromosomes in establishing sex differences in behaviours. 

References

Arnold AP (2020a) Sexual differentiation of brain and other tissues: Five questions for the next 50 years. Hormones and Behavior, 120, 104691. https://doi.org/10.1016/j.yhbeh.2020.104691

Arnold AP (2020b) Four Core Genotypes and XY* mouse models: Update on impact on SABV research. Neuroscience & Biobehavioral Reviews, 119, 1–8. https://doi.org/10.1016/j.neubiorev.2020.09.021

Arnold AP, Chen X (2009) What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Frontiers in Neuroendocrinology, 30, 1–9. https://doi.org/10.1016/j.yfrne.2008.11.001

Gatewood JD, Wills A, Shetty S, Xu J, Arnold AP, Burgoyne PS, Rissman EF (2006) Sex Chromosome Complement and Gonadal Sex Influence Aggressive and Parental Behaviors in Mice. Journal of Neuroscience, 26, 2335–2342. https://doi.org/10.1523/JNEUROSCI.3743-05.2006

Heitzmann LD, Challe M, Perez J, Castell L, Galibert E, Martin A, Valjent E, Veyrunes F (2022) Genotypic sex shapes maternal care in the African Pygmy mouse, Mus minutoides. bioRxiv, 2022.04.05.487174, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.04.05.487174

Petty JMA, Drea CM (2015) Female rule in lemurs is ancestral and hormonally mediated. Scientific Reports, 5, 9631. https://doi.org/10.1038/srep09631

Saunders PA, Perez J, Rahmoun M, Ronce O, Crochet P-A, Veyrunes F (2014) Xy Females Do Better Than the Xx in the African Pygmy Mouse, Mus Minutoides. Evolution, 68, 2119–2127. https://doi.org/10.1111/evo.12387

Saunders PA, Perez J, Ronce O, Veyrunes F (2022) Multiple sex chromosome drivers in a mammal with three sex chromosomes. Current Biology, 32, 2001-2010.e3. https://doi.org/10.1016/j.cub.2022.03.029

Veyrunes F, Perez J, Heitzmann L, Saunders PA, Givalois L (2022) Separating the effects of sex hormones and sex chromosomes on behavior in the African pygmy mouse Mus minutoides, a species with XY female sex reversal. bioRxiv, 2022.07.11.499546. https://doi.org/10.1101/2022.07.11.499546

Genotypic sex shapes maternal care in the African Pygmy mouse, Mus minutoidesLouise D Heitzmann, Marie Challe, Julie Perez, Laia Castell, Evelyne Galibert, Agnes Martin, Emmanuel Valjent, Frederic Veyrunes<p>Sexually dimorphic behaviours, such as parental care, have long been thought to be driven mostly, if not exclusively, by gonadal hormones. In the past two decades, a few studies have challenged this view, highlighting the direct influence of th...Behavior & Social Evolution, Evolutionary Ecology, Reproduction and SexGabriel Marais2022-04-08 20:09:58 View
24 Oct 2022
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Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscura

The other side of the evolution of heat tolerance: correlated responses in metabolism and life-history traits

Recommended by and ORCID_LOGO based on reviews by Marija Savić Veselinović and 1 anonymous reviewer

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

Evolutionary responses of energy metabolism, development, and reproduction to artificial selection for increasing heat tolerance in Drosophila subobscuraAndres Mesas, Luis E. Castaneda<p>Adaptations to warming conditions exhibited by ectotherms include increasing heat tolerance but also metabolic changes to reduce maintenance costs (metabolic depression), which can allow them to redistribute the energy surplus to biological fun...Adaptation, Evolutionary Ecology, Experimental Evolution, Life HistoryInês Fragata2022-02-08 01:05:50 View
11 Oct 2022
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The Eukaryotic Last Common Ancestor Was Bifunctional for Hopanoid and Sterol Production

Gene family analysis suggests new evolutionary scenario for sterol and hopanoid biomarkers

Recommended by based on reviews by Samuel Abalde, Denis Baurain and Jose Ramon Pardos-Blas

Sterols and hopanoids are sometimes used as biomarkers to infer the origin of certain groups of organisms. Traditionally, hopanoid-derived products in ancient rocks have been considered to indicate the presence of bacteria, whereas sterol derivatives have been considered to be exclusive to eukaryotes. However, a closer look at the topic reveals a rather complex distribution of either compound in both bacteria and eukaryotes. (1). The known biosynthetic pathways for sterols and hopanoids are similar but diverge at a critical step where two different enzymes are used: squalene-hopene cyclase (SHC) and oxidosqualene cyclase (OSC), the latter requiring oxygen. These two enzymes belong to the same gene family, whose complex evolutionary history is difficult to reconcile with the known species phylogeny.

In this study (2), Dr. Warren R. Francis revisits the evolution of this gene family using an extended dataset with a broader taxonomic representation. In contrast to the traditional representation of the tree rooted between SHC and OSC paralogs (i.e., based on function), the author proposes that rooting the tree within bacterial SHCs and assuming a secondary origin of OSC is more parsimonious. This postulates SHC to be the ancestral function –retained in many extant bacteria and some eukaryotes– and OSC to have emerged later within bacteria –currently being mostly present in eukaryotes–. The reconstructed evolutionary history is arguably complex and can only be reconciled with the species' phylogeny by invoking many secondary losses. These losses are considered likely because many extant species acquire sterols and hopanoids by diet and lack one or both enzymes. Some cases of recent horizontal gene transfer are also proposed.

In contrast to the dichotomy between bacterial SHCs and eukaryote OSCs, the new proposed scenario suggests that the eukaryote ancestor likely inherited both enzymes from bacteria and thus could be able to synthesize both sterols and hopanoids. Under this hypothesis, not only bacteria but also eukaryotes could be responsible for the hopane found in old rocks. This agrees with eukaryote fossils dating back to more than 1 billion years ago (3). Also, the observed increase of sterane levels in rocks ~600-700 million years old cannot be associated with the origin of eukaryotes, which is a much older event, but could rather reflect changes in atmospheric oxygen levels because oxygen is required for the synthesis of sterols by OSC.

References

1. Santana-Molina C, Rivas-Marin E, Rojas AM, Devos DP (2020) Origin and Evolution of Polycyclic Triterpene Synthesis. Molecular Biology and Evolution, 37, 1925–1941. https://doi.org/10.1093/molbev/msaa054

2. Francis WR (2022) The Eukaryotic Last Common Ancestor Was Bifunctional for Hopanoid and Sterol Production. Preprints, 2020040186, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology.  https://doi.org/10.20944/preprints202004.0186.v5

3. Butterfield NJ (2000) Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology, 26, 386–404.  https://doi.org/10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2

The Eukaryotic Last Common Ancestor Was Bifunctional for Hopanoid and Sterol ProductionWarren R Francis<p>Steroid and hopanoid biomarkers can be found in ancient rocks and may give a glimpse of what life was present at that time. Sterols and hopanoids are produced by two related enzymes, though the evolutionary history of this protein family is com...Bioinformatics & Computational Biology, Evolutionary Ecology, Molecular Evolution, Paleontology, Phylogenetics / PhylogenomicsIker Irisarri2021-01-13 16:03:29 View
06 Oct 2022
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Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch.

Evolution of sperm morphology in Daphnia within a phyologenetic context

Recommended by based on reviews by Renate Matzke-Karasz and 1 anonymous reviewer

In this study sperm morphology is studied in 15 Daphnia species and the morphological data are mapped on a Daphnia phylogeny. The authors found that despite the internal fertilization mode, Daphnia have among the smallest sperm recorded, as would be expected with external fertilization. The authors also conclude that increase in sperm length has evolved twice, that sperm encapsulation has been lost in a clade, and that this clade has very polymorphic sperm with long, and often numerous, filopodia.

Daphnia is an interesting model to study sperm morphology because the biology of sexual reproduction is often ignored in (cyclical) parthenogenetic species. Daphnia is part of the very diverse and successful group of cladocerans with cyclical parthenogenetic reproduction. The success of this reproduction mode is reflected in the known 620 species that radiated within this order, this is more than half of the known Branchiopod species diversity and the estimated number of cladoceran species is even two to four times higher (Forró et al. 2008). Looking at this particular model with a good phylogeny and some particularity in the mode of fertilization/reproduction, has thus a large value. Most Daphnia species are cyclical parthenogenetic and switch between sexual and asexual reproduction depending on the environmental conditions. Within the genus Daphnia, evolution to obligate asexuality has evolved in at least four independent occasions by three different mechanisms: (i) obligate parthenogenesis through hybridisation with or without polyploidy, (ii) asexuality has been acquired de novo in some populations and (iii) in certain lineages females reproduce by obligate parthenogenesis, whereas the clonally propagated males produce functional haploid sperm that allows them to breed with sexual females of normal cyclically parthenogenetic lineages (more on this in Decaestecker et al. 2009).

This study is made in the context of a body of research on the evolution of one of the most fundamental and taxonomically diverse cell types. There is surprisingly little known about the adaptive value underlying their morphology because it is very difficult to test this experimentally.  Studying sperm morphology across species is interesting to study evolution itself because it is a "simple trait". As the authors state: The understanding of the adaptive value of sperm morphology, such as length and shape, remains largely incomplete (Lüpold & Pitnick, 2018). Based on phylogenetic analyses across the animal kingdom, the general rule seems to be that fertilization mode (i.e. whether eggs are fertilized within or outside the female) is a key predictor of sperm length (Kahrl et al., 2021). There is a trade-off between sperm number and length (Immler et al., 2011). This study reports on one of the smallest sperm recorded despite the fertilization being internal. The brood pouch in Daphnia is an interesting particularity as fertilisation occurs internally, but it is not disconnected from the environment. It is also remarkable that there are two independent evolution lines of sperm size in this group. It suggests that those traits have an adaptive value. 

References

Decaestecker E, De Meester L, Mergeay J (2009) Cyclical Parthenogenesis in Daphnia: Sexual Versus Asexual Reproduction. In: Lost Sex: The Evolutionary Biology of Parthenogenesis (eds Schön I, Martens K, Dijk P), pp. 295–316. Springer Netherlands, Dordrecht. https://doi.org/10.1007/978-90-481-2770-2_15

Duneau David, Möst M, Ebert D (2022) Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch. bioRxiv, 2020.01.31.929414, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.01.31.929414

Forró L, Korovchinsky NM, Kotov AA, Petrusek A (2008) Global diversity of cladocerans (Cladocera; Crustacea) in freshwater. Hydrobiologia, 595, 177–184. https://doi.org/10.1007/s10750-007-9013-5

Immler S, Pitnick S, Parker GA, Durrant KL, Lüpold S, Calhim S, Birkhead TR (2011) Resolving variation in the reproductive tradeoff between sperm size and number. Proceedings of the National Academy of Sciences, 108, 5325–5330. https://doi.org/10.1073/pnas.1009059108

Kahrl AF, Snook RR, Fitzpatrick JL (2021) Fertilization mode drives sperm length evolution across the animal tree of life. Nature Ecology & Evolution, 5, 1153–1164. https://doi.org/10.1038/s41559-021-01488-y

Lüpold S, Pitnick S (2018) Sperm form and function: what do we know about the role of sexual selection? Reproduction, 155, R229–R243. https://doi.org/10.1530/REP-17-0536

Evolution of sperm morphology in a crustacean genus with fertilization inside an open brood pouch.Duneau, David; Moest, Markus; Ebert, Dieter<p style="text-align: justify;">Sperm is the most fundamental male reproductive feature. It serves the fertilization of eggs and evolves under sexual selection. Two components of sperm are of particular interest, their number and their morphology....Evolutionary Ecology, Morphological Evolution, Reproduction and Sex, Sexual SelectionEllen Decaestecker2020-05-30 22:54:15 View
05 Oct 2022
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Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks

Testing for phylogenetic signal in species interaction networks

Recommended by based on reviews by Joaquin Calatayud and Thomas Guillerme

Species are immersed within communities in which they interact mutualistically, as in pollination or seed dispersal, or nonreciprocally, such as in predation or parasitism, with other species and these interactions play a paramount role in shaping biodiversity (Bascompte and Jordano 2013). Researchers have become increasingly interested in the processes that shape these interactions and how these influence community structure and responses to disturbances. Species interactions are often described using bipartite interaction networks and one important question is how the evolutionary history of the species involved influences the network, including whether there is phylogenetic signal in interactions, in other words whether closely related species interact with other closely related species (Bascompte and Jordano 2013, Perez-Lamarque et al. 2022). To address this question different approaches, correlative and model-based, have been developed to test for phylogenetic signal in interactions, although comparative analyses of the performance of these different metrics are lacking. In their article Perez-Lamarque et al. (2022) set out to test the statistical performance of two widely-used methods, Mantel tests and Phylogenetic Bipartite Linear Models (PBLM; Ives and Godfray 2006) using simulations. Phylogenetic signal is measured as the degree to which distance to the nearest common ancestor predicts the observed similarity in trait values among species. In species interaction networks, the data are actually the between-species dissimilarity among interacting species (Perez-Lamarque et al. 2022), and typical approaches to test for phylogenetic signal cannot be used. However, the Mantel test provides a useful means of analyzing the correlation between two distance matrices, the between-species phylogenetic distance and the between-species dissimilarity in interactions. The PBLM approach, on the other hand, assumes that interactions between species are influenced by unobserved traits that evolve along the phylogenies following a given phenotypic evolution model and the parameters of this model are interpreted in terms of phylogenetic signal (Ives and Godfray 2006). Perez-Lamarque et al (2022) found that the model-based PBLM approach has a high type-I error rate, in other words it often detected phylogenetic signal when there was none. The simple Mantel test was found to present a low type-I error rate and moderate statistical power. However, it tended to overestimate the degree to which species interact with dissimilar partners. In addition to the aforementioned analyses, the authors also tested whether the simple Mantel test was able to detect phylogenetic signal in interactions among species within a given clade in the phylogeny, as phylogenetic signal in species interactions may be localized within specific clades. The article concludes with general guidelines for users wishing to test phylogenetic signal in their interaction networks and illustrates them with an example of an orchid-mycorrhizal fungus network from the oceanic island of La Réunion (Martos et al 2012). This broadly accessible article provides a valuable analysis of the performance of tests of phylogenetic signal in interaction networks enabling users to make informed choices of the analytical methods they wish to employ, and provide useful and detailed guidelines. Therefore, the work should be of broad interest to researchers studying species interactions.  

References

Bascompte J, Jordano P (2013) Mutualistic Networks. Princeton University Press. https://doi.org/10.1515/9781400848720

Ives AR, Godfray HCJ (2006) Phylogenetic Analysis of Trophic Associations. The American Naturalist, 168, E1–E14. https://doi.org/10.1086/505157

Martos F, Munoz F, Pailler T, Kottke I, Gonneau C, Selosse M-A (2012) The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Molecular Ecology, 21, 5098–5109. https://doi.org/10.1111/j.1365-294X.2012.05692.x

Perez-Lamarque B, Maliet O, Pichon B, Selosse M-A, Martos F, Morlon H (2022) Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks. bioRxiv, 2021.08.30.458192, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.08.30.458192

Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks Benoît Perez-Lamarque, Odile Maliet, Benoît Pichon, Marc-André Selosse, Florent Martos, Hélène Morlon<p style="text-align: justify;">Whether interactions between species are conserved on evolutionary time-scales has spurred the development of both correlative and process-based approaches for testing phylogenetic signal in interspecific interactio...Evolutionary Ecology, Species interactionsAlejandro Gonzalez Voyer2022-03-10 13:48:15 View
29 Sep 2022
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How many sirtuin genes are out there? evolution of sirtuin genes in vertebrates with a description of a new family member

Making sense of vertebrate sirtuin genes

Recommended by based on reviews by Filipe Castro, Nicolas Leurs and 1 anonymous reviewer

Sirtuin proteins are class III histone deacetylases that are involved in a variety of fundamental biological functions mostly related to aging. These proteins are located in different subcellular compartments and are associated with different biological functions such as metabolic regulation, stress response, and cell cycle control [1]. In mammals, the sirtuin gene family is composed of seven paralogs (SIRT1-7) grouped into four classes [2]. Due to their involvement in maintaining cell cycle integrity, sirtuins have been studied as a way to understand fundamental mechanisms governing longevity [1]. Indeed, the downregulation of sirtuin genes with aging seems to explain much of the pathophysiology that accumulates with aging [3]. Biomedical studies have thus explored the potential therapeutic implications of sirtuins [4] but whether they can effectively be used as molecular targets for the treatment of human diseases remains to be demonstrated [1]. Despite this biomedical interest and some phylogenetic analyses of sirtuin paralogs mostly conducted in mammals, a comprehensive evolutionary analysis of the sirtuin gene family at the scale of vertebrates was still lacking.

In this preprint, Opazo and collaborators [5] took advantage of the increasing availability of whole-genome sequences for species representing all main groups of vertebrates to unravel the evolution of the sirtuin gene family. To do so, they undertook a phylogenomic approach in its original sense aimed at improving functional predictions by evolutionary analysis [6] in order to inventory the full vertebrate sirtuin gene repertoire and reconstruct its precise duplication history. Harvesting genomic databases, they extracted all predicted sirtuin proteins and performed phylogenetic analyses based on probabilistic inference methods. Maximum likelihood and Bayesian analyses resulted in well-resolved and congruent phylogenetic trees dividing vertebrate sirtuin genes into three major clades. These analyses also revealed an additional eighth paralog that was previously overlooked because of its restricted phyletic distribution. This newly identified sirtuin family member (named SIRT8) was recovered with unambiguous statistical support as a sister-group to the SIRT3 clade. Comparative genomic analyses based on conserved gene synteny confirmed that SIRT8 was present in all sampled non-amniote vertebrate genomes (cartilaginous fish, bony fish, coelacanth, lungfish, and amphibians) except cyclostomes. SIRT8 has thus most likely been lost in the last common ancestor of amniotes (mammals, reptiles, and birds). Discovery of such previously unknown genes in vertebrates is not completely surprising given the plethora of high-quality genomes now available. However, this study highlights the importance of considering a broad taxonomic sampling to infer evolutionary patterns of gene families that have been mostly studied in mammals because of their potential importance for human biology.

Based on its phylogenetic position as closely related to SIRT3 within class I, it could be predicted that the newly identified SIRT8 paralog likely has a deacetylase activity and is probably located in mitochondria. To test these evolutionary predictions, Opazo and collaborators [5] conducted further bioinformatics analyses and functional experiments using the elephant shark (Callorhinchus milii) as a model species. RNAseq expression data were analyzed to determine tissue-specific transcription of sirtuin genes in vertebrates, including SIRT8 found to be mainly expressed in the ovary, which suggests a potential role in biological processes associated with reproduction. The elephant shark SIRT8 protein sequence was used with other vertebrates for comparative analyses of protein structure modeling and subcellular localization prediction both pointing to a probable mitochondrial localization. The protein localization and its function were further characterized by immunolocalization in transfected cells, and enzymatic and functional assays, which all confirmed the prediction that SIRT8 proteins are targeted to the mitochondria and have deacetylase activity. The extensive experimental efforts made in this study to shed light on the function of this newly discovered gene are both rare and highly commendable.

Overall, this work by Opazo and collaborators [5] provides a comprehensive phylogenomic study of the sirtuin gene family in vertebrates based on detailed evolutionary analyses using state-of-the-art phylogenetic reconstruction methods. It also illustrates the power of adopting an integrative comparative approach supplementing the reconstruction of the duplication history of the gene family with complementary functional experiments in order to elucidate the function of the newly discovered SIRT8 family member. These results provide a reference phylogenetic framework for the evolution of sirtuin genes and the further functional characterization of the eight vertebrate paralogs with potential relevance for understanding the cellular biology of aging and its associated diseases in human.

References

[1] Vassilopoulos A, Fritz KS, Petersen DR, Gius D (2011) The human sirtuin family: Evolutionary divergences and functions. Human Genomics, 5, 485. https://doi.org/10.1186/1479-7364-5-5-485

[2] Yamamoto H, Schoonjans K, Auwerx J (2007) Sirtuin Functions in Health and Disease. Molecular Endocrinology, 21, 1745–1755. https://doi.org/10.1210/me.2007-0079

[3] Morris BJ (2013) Seven sirtuins for seven deadly diseases ofaging. Free Radical Biology and Medicine, 56, 133–171. https://doi.org/10.1016/j.freeradbiomed.2012.10.525

[4] Bordo D Structure and Evolution of Human Sirtuins. Current Drug Targets, 14, 662–665. http://dx.doi.org/10.2174/1389450111314060007

[5] Opazo JC, Vandewege MW, Hoffmann FG, Zavala K, Meléndez C, Luchsinger C, Cavieres VA, Vargas-Chacoff L, Morera FJ, Burgos PV, Tapia-Rojas C, Mardones GA (2022) How many sirtuin genes are out there? evolution of sirtuin genes in vertebrates with a description of a new family member. bioRxiv, 2020.07.17.209510, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology.  https://doi.org/10.1101/2020.07.17.209510

[6] Eisen JA (1998) Phylogenomics: Improving Functional Predictions for Uncharacterized Genes by Evolutionary Analysis. Genome Research, 8, 163–167. https://doi.org/10.1101/gr.8.3.163

How many sirtuin genes are out there? evolution of sirtuin genes in vertebrates with a description of a new family memberJuan C. Opazo, Michael W. Vandewege, Federico G. Hoffmann, Kattina Zavala, Catalina Meléndez, Charlotte Luchsinger, Viviana A. Cavieres, Luis Vargas-Chacoff, Francisco J. Morera, Patricia V. Burgos, Cheril Tapia-Rojas, Gonzalo A. Mardones<p style="text-align: justify;">Studying the evolutionary history of gene families is a challenging and exciting task with a wide range of implications. In addition to exploring fundamental questions about the origin and evolution of genes, disent...Molecular EvolutionFrédéric Delsuc Filipe Castro, Anonymous, Nicolas Leurs2022-05-12 16:06:04 View
15 Sep 2022
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Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects

Spreading the risk of reproductive failure when the environment is unpredictable and ephemeral

Recommended by based on reviews by Thomas Haaland and Zoltan Radai

Many species breed in environments that are unpredictable, for instance in terms of the availability of resources needed to raise the offspring. Organisms might respond to such spatial and temporal unpredictability by adopting plastic responses to adjust their reproductive investment according to perceived cues of environmental quality. Some species such as the amphibians might also face the problem of ephemeral habitats, when the ponds where they breed have a chance of drying up before metamorphosis has occurred. In this case, maximizing long-term fitness might involve a strategy of spreading the risk, even though the reproductive success of a single reproductive bout might be lower. Understanding how animals (and plants) get adapted to stochastic environments is particularly crucial in the current context of rapid environmental changes.

In this article, Jourdan-Pineau et al. report the results of field surveys of the Parsley Frog (Pelodytes punctatus) in Southern France. This frog has peculiar breeding phenology with females breeding in autumn and spring. The authors provide quite an extensive amount of information on the reproductive success of eggs laid in each season and the possible ecological factors accounting for differences between seasons. Although the presence of interspecific competitors and predators does not seem to account for pond-specific reproductive success, the survival of tadpoles hatching from eggs laid in spring is severely impaired when tadpoles from the autumn cohort have managed to survive. This intraspecific competition takes the form of a “priority” effect where tadpoles from the autumn cohort outcompete the smaller larvae from the spring cohort. Given this strong priority effect, one might tentatively predict that females laying in spring should avoid ponds with tadpoles from the autumn cohort. Surprisingly, however, the authors did not find any evidence for such avoidance, which might indicate strong constraints on the availability of ponds where females might possibly lay.

Assuming that each female can indeed lay both in autumn and spring, how is this bimodal phenology maintained? Would not be worthier to allocate all the eggs to the autumn (or the spring) laying season? Eggs laid in autumn and spring have to face different environmental hazards, reducing their hatching success and the probability to produce metamorphs (for instance, tadpoles hatching from eggs laid in autumn have to overwinter which might be a particularly risky phase).             

Jourdan-Pineau and coworkers addressed this question by adapting a bet-hedging model that was initially developed to investigate the strategy of allocation into seed dormancy of annual plants (Cohen 1966) to the case of the bimodal phenology of the Parsley Frog. By feeding the model with the parameter values obtained from the field surveys, they found that the two breeding strategies (laying in autumn and in spring) can coexist as long as the probability of breeding success in the autumn cohort is between 20% and 80% (the range of values allowing the coexistence of a bimodal phenology shrinking a little bit when considering that frogs can reproduce 5 times during their lifespan instead of three times).

This paper provides a very nice illustration of the importance of combining approaches (here field monitoring to gather data that can be used to feed models) to understand the evolution of peculiar breeding strategies. Although future work should attempt to gather individual-based data (in addition to population data), this work shows that spreading the risk can be an adaptive strategy in environments characterized by strong stochastic variation.

References

Cohen D (1966) Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology, 12, 119–129. https://doi.org/10.1016/0022-5193(66)90188-3

Jourdan-Pineau H., Crochet P.-A., David P. (2022) Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effects. bioRxiv, 2022.02.24.481784, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.02.24.481784

Bimodal breeding phenology in the Parsley Frog Pelodytes punctatus as a bet-hedging strategy in an unpredictable environment despite strong priority effectsHelene Jourdan-Pineau, Pierre-Andre Crochet, Patrice David<p style="text-align: justify;">When environmental conditions are unpredictable, expressing alternative phenotypes spreads the risk of failure, a mixed strategy called bet-hedging. In the southern part of its range, the Parsley Frog <em>Pelodytes ...Adaptation, Evolutionary Ecology, Life HistoryGabriele Sorci2022-02-28 11:53:00 View