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11 May 2023
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Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineages

Flexibility in Aphid Endosymbiosis: Dual Symbioses Have Evolved Anew at Least Six Times

Recommended by based on reviews by Alex C. C. Wilson and 1 anonymous reviewer

In this intriguing study (Manzano-Marín et al. 2022) by Alejandro Manzano-Marin and his colleagues, the association between aphids and their symbionts is investigated through meta-genomic analysis of new samples. These associations have been previously described as leading to fascinating genomic evolution in the symbiont (McCutcheon and Moran 2012). The bacterial genomes exhibit a significant reduction in size and the range of functions performed. They typically lose the ability to produce many metabolites or biobricks created by the host, and instead, streamline their metabolism by focusing on the amino acids that the host cannot produce. This level of co-evolution suggests a stable association between the two partners.

However, the new data suggests a much more complex pattern as multiple independent acquisitions of co-symbionts are observed. Co-symbiont acquisition leads to a partition of the functions carried out on the bacterial side, with the new co-symbiont taking over some of the functions previously performed by Buchnera. In most cases, the new co-symbiont also brings the ability to produce B1 vitamin. Various facultative symbiotic taxa are recruited to be co-symbionts, with the frequency of acquisition related to the bacterial niche and lifestyle.
Despite this diversity of associations, the evolution of co-obligate symbiosis in aphids commonly involves just a handful of nutritional pathways. These include tryptophan biosynthesis (twice), histidine biosynthesis, riboflavin biosynthesis (six times), and biotin biosynthesis (five times). Microscopy analyses suggest that some co-symbionts colonize different bacteriocytes. Yet, a few traces of horizontal gene transfers in Buchnera suggest that some contact with other bacteria may occasionally occur.
The emergence of multiple co-symbioses highlights the success of a "menage à trois". However, this success is achieved by adding a new co-symbiont to an already established pair. It is possible that the slow but irreversible decay of the bacterial genome under symbiosis may lead to a degradation of the partnership, creating a niche for the acquisition of new bacteria to maintain the symbiosis.

REFERENCES

Manzano-Marín, Alejandro, Armelle Coeur D’acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, and Emmanuelle Jousselin. 2023. “Co-Obligate Symbioses Have Repeatedly Evolved across Aphids, but Partner Identity and Nutritional Contributions Vary across Lineages.” bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.08.28.505559.

McCutcheon, John P., and Nancy A. Moran. 2012. “Extreme Genome Reduction in Symbiotic Bacteria.” Nature Reviews Microbiology 10 (1): 13–26. https://doi.org/10.1038/nrmicro2670.

Co-obligate symbioses have repeatedly evolved across aphids, but partner identity and nutritional contributions vary across lineagesAlejandro Manzano-Marín, Armelle Coeur d'acier, Anne-Laure Clamens, Corinne Cruaud, Valérie Barbe, Emmanuelle Jousselin<p style="text-align: justify;">Aphids are a large family of phloem-sap feeders. They typically rely on a single bacterial endosymbiont, <em>Buchnera aphidicola</em>, to supply them with essential nutrients lacking in their diet. This association ...Genome Evolution, Other, Species interactionsOlivier Tenaillon2022-11-16 10:13:37 View
25 Sep 2023
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Random genetic drift sets an upper limit on mRNA splicing accuracy in metazoans

The drift barrier hypothesis and the limits to alternative splicing accuracy

Recommended by ORCID_LOGO based on reviews by Lars M. Jakt and 2 anonymous reviewers

Accurate information flow is central to living systems. The continuity of genomes through generations as well as the reproducible functioning and survival of the individual organisms require a faithful information transfer during replication, transcription and translation. The differential efficiency of natural selection against “mistakes” results in decreasing fidelity rates for replication, transcription and translation. At each level in the information flow chain (replication, transcription, translation), numerous complex molecular systems have evolved and been selected for preventing, identifying and, when possible, correcting or removing such “mistakes” arising during information transfer.

However, fidelity cannot be improved ad infinitum. First, because of the limits imposed by the physical nature of the processes of copying and recoding information over different molecular supports: all mechanisms ensuring fidelity during biological information transfer ultimately rely on chemical kinetics and thermodynamics. The more accurate a copying process is, the lower the synthesis rate and the higher the energetic cost of correcting errors. Second, because of the limits imposed by random genetic drift: natural selection cannot effectively act on an allele that contributes with a small differential advantage unless effective population size is large. If s <1/Ne (or s <1/(2Ne) in diploids) the allele frequency in the population is de facto subject to neutral drift processes.

In their preprint “Random genetic drift sets an upper limit on mRNA splicing accuracy in metazoans”, Bénitière, Necsulea and Duret explore the validity of this last mentioned “drift barrier” hypothesis for the case study of alternative splicing diversity in eukaryotes (Bénitière et al. 2022). Splicing refers to an ensemble of eukaryotic molecular processes mediated by a large number of proteins and ribonucleoproteins and involving nucleotide sequence recognition, that uses as a molecular substrate a precursor messenger RNA (mRNA), directly transcribed from the DNA, and produces a mature mRNA by removing introns and joining exons (Chow et al. 1977). Alternative splicing refers to the case in which different molecular species of mature mRNAs can be produced, either by cis-splicing processes acting on the same precursor mRNA, e.g. by varying the presence/absence of different exons or by varying the exon-exon boundaries, or by trans-splicing processes, joining exons from different precursor mRNA molecules.

The diversity of mRNA molecular species generated by alternative splicing enlarges the molecular phenotypic space that can be generated from the same genotype. In humans, alternative splicing occurs in around 95% of the ca. 20,000 genes, resulting in ca. 100,000 medium-to-high abundance transcripts (Pan et al. 2008). In multicellular organisms, the frequency of alternatively spliced mRNAs varies between tissues and across ontogeny, often in a switch-like pattern (Wang et al. 2008). In the molecular and cell biology community, it is commonly accepted that splice variants contribute with specific functions (Marasco and Kornblihtt 2023) although there exists a discussion around the functional nature of low-frequency splice variants (see for instance the debate between Tress et al. 2017 and Blencowe 2017). The origin, diversity, regulation and evolutionary advantage of alternative splicing constitutes thus a playground of the selectionist-neutralist debate, with one extreme considering that most splice variants are mere “mistakes” of the splicing process (Pickrell et al. 2010), and the other extreme considering that alternative splicing is at the core of complexity in multicellular organisms, as it increases the genome coding potential and allows for a large repertoire of cell types (Chen et al. 2014).

In their manuscript, Bénitière, Necsulea and Duret set the cursor towards the neutralist end of the gradient and test the hypothesis of whether the high alternative splice rate in “complex” organisms corresponds to a high rate of splicing “mistakes”, arising from the limit imposed by the drift barrier effect on the power of natural selection to increase accuracy (Bush et al. 2017). In their preprint, the authors convincingly show that in metazoans a fraction of the variation of alternative splicing rate is explained by variation in proxies of population size, so that species with smaller Ne display higher alternative splice rates. They communicate further that abundant splice variants tend to preserve the reading frame more often than low-frequency splice variants, and that the nucleotide splice signals in abundant splice variants display stronger evidence of purifying selection than those in low-frequency splice variants. From all the evidence presented in the manuscript, the authors interpret that “variation in alternative splicing rate is entirely driven by variation in the efficacy of selection against splicing errors”.

The authors honestly present some of the limitations of the data used for the analyses, regarding i) the quality of the proxies used for Ne (i.e. body length, longevity and dN/dS ratio); ii) the heterogeneous nature of the RNA sequencing datasets (full organisms, organs or tissues; different life stages, sexes or conditions); and iii) mostly short RNA reads that do not fully span individual introns. Further, data from bacteria do not verify the herein communicated trends, as it has been shown that bacterial species with low population sizes do not display higher transcription error rates (Traverse and Ochman 2016). Finally, it will be extremely interesting to introduce a larger evolutionary perspective on alternative splicing rates encompassing unicellular eukaryotes, in which an intriguing interplay between alternative splicing and gene duplication has been communicated (Hurtig et al. 2020).

The manuscript from Bénitière, Necsulea and Duret makes a significant advance to our understanding of the diversity, the origin and the physiology of post-transcriptional and post-translational mechanisms by emphasising the fundamental role of non-adaptive evolutionary processes and the upper limits to splicing accuracy set by genetic drift.

References

Bénitière F, Necsulea A, Duret L. 2023. Random genetic drift sets an upper limit on mRNA splicing accuracy in metazoans. bioRxiv, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.12.09.519597 

Blencowe BJ. 2017. The Relationship between Alternative Splicing and Proteomic Complexity. Trends Biochem Sci 42:407–408. https://doi.org/10.1016/j.tibs.2017.04.001

Bush SJ, Chen L, Tovar-Corona JM, Urrutia AO. 2017. Alternative splicing and the evolution of phenotypic novelty. Philos Trans R Soc Lond B Biol Sci 372:20150474. https://doi.org/10.1098/rstb.2015.0474

Chen L, Bush SJ, Tovar-Corona JM, Castillo-Morales A, Urrutia AO. 2014. Correcting for differential transcript coverage reveals a strong relationship between alternative splicing and organism complexity. Mol Biol Evol 31:1402–1413. https://doi.org/10.1093/molbev/msu083

Chow LT, Gelinas RE, Broker TR, Roberts RJ. 1977. An amazing sequence arrangement at the 5’ ends of adenovirus 2 messenger RNA. Cell 12:1–8. https://doi.org/10.1016/0092-8674(77)90180-5

Hurtig JE, Kim M, Orlando-Coronel LJ, Ewan J, Foreman M, Notice L-A, Steiger MA, van Hoof A. 2020. Origin, conservation, and loss of alternative splicing events that diversify the proteome in Saccharomycotina budding yeasts. RNA 26:1464–1480. https://doi.org/10.1261/rna.075655.120

Marasco LE, Kornblihtt AR. 2023. The physiology of alternative splicing. Nat Rev Mol Cell Biol 24:242–254. https://doi.org/10.1038/s41580-022-00545-z

Pan Q, Shai O, Lee LJ, Frey BJ, Blencowe BJ. 2008. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40:1413–1415. https://doi.org/10.1038/ng.259

Pickrell JK, Pai AA, Gilad Y, Pritchard JK. 2010. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 6:e1001236. https://doi.org/10.1371/journal.pgen.1001236

Traverse CC, Ochman H. 2016. Conserved rates and patterns of transcription errors across bacterial growth states and lifestyles. Proc Natl Acad Sci U S A 113:3311–3316. https://doi.org/10.1073/pnas.1525329113

Tress ML, Abascal F, Valencia A. 2017. Alternative Splicing May Not Be the Key to Proteome Complexity. Trends Biochem Sci 42:98–110. https://doi.org/10.1016/j.tibs.2016.08.008

Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476. https://doi.org/10.1038/nature07509

Random genetic drift sets an upper limit on mRNA splicing accuracy in metazoansFlorian Benitiere, Anamaria Necsulea, Laurent Duret<p style="text-align: justify;">Most eukaryotic genes undergo alternative splicing (AS), but the overall functional significance of this process remains a controversial issue. It has been noticed that the complexity of organisms (assayed by the nu...Bioinformatics & Computational Biology, Genome Evolution, Molecular Evolution, Population Genetics / GenomicsIgnacio BravoAnonymous2022-12-12 14:00:01 View
30 Jun 2023
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How do monomorphic bacteria evolve? The Mycobacterium tuberculosis complex and the awkward population genetics of extreme clonality

How the tubercle bacillus got its genome: modernising, modelling, and making sense of the stories we tell

Recommended by based on reviews by 2 anonymous reviewers

In this instructive review, Stritt and Gagneux offer a balanced perspective on the evolutionary forces shaping Mycobacterium tuberculosis and make the case that our instinct for storytelling be balanced with quantitative models. M. tuberculosis is perhaps the best-known clonal bacterial pathogen – evolving largely in the absence of horizontal gene transfer. Its genome is full of puzzling patterns, including much higher GC content than most intracellular pathogens (which suggests efficient selection to resist AT-skewed mutational bias) but a very high ratio of nonsynonymous to synonymous substitution rates (dN/dS ~ 0.5, typically interpreted as weak selection against deleterious amino acid changes). 

The authors offer alternative explanations for these patterns, framing the question: is M. tuberculosis evolution shaped mainly by drift or by efficient selection? They propose that this question can only be answered by accounting for the pathogen’s extreme clonality. A clonal lifestyle can have its advantages, for example when adaptations must arise in a particular order (Kondrashov and Kondrashov 2001). An important disadvantage highlighted by the authors are linkage effects: without recombination to shuffle them up, beneficial mutations are linked to deleterious mutations in the same genome (hitchhiking) and purging deleterious mutations also purges neutral diversity across the genome (background selection). The authors propose the latter – efficient purifying selection and strong linkage – as an explanation for the low genetic diversity observed in M. tuberculosis. This is of course not exclusive of other related explanations, such as clonal interference (Gerrish and Lenski 1998). They also champion the use of forward evolutionary simulations (Haller and Messer 2019) to model the interplay between selection, recombination, and demography as a powerful alternative to traditional backward coalescent models.

At times, Stritt and Gagneux are pessimistic about our existing methods – arguing that dN/dS and homoplasies “tell us little about the frequency and strength of selection.” Even though I favour a more optimistic view, I fully agree that our traditional population genetic metrics are sensitive to a slew of different deviations from a standard neutral evolution model and must be interpreted with caution. As I and others have argued, the extent of recombination (measured as the amount of linkage in a genome) is a key factor in determining how best to test for natural selection (Shapiro et al. 2009) and to conduct genotype-phenotype association studies (Chen and Shapiro 2021) in microbes. While this article is focused on the well-studied M. tuberculosis complex, there are many parallels with other clonal bacteria, including pathogens and symbionts. Whatever your favourite bug, we must all be careful to make sure the stories we tell about them are not “just so tales” but are supported, to the extent possible, by data and quantitative models.

References

Chen, Peter E., and B. Jesse Shapiro. 2021. "Classic Genome-Wide Association Methods Are Unlikely to Identify Causal Variants in Strongly Clonal Microbial Populations." bioRxiv. 
https://doi.org/10.1101/2021.06.30.450606
 
Gerrish, P. J., and R. E. Lenski. 1998. "The Fate of Competing Beneficial Mutations in an Asexual Population." Genetica 102-103 (1-6): 127-44.
https://doi.org/10.1023/A:1017067816551
 
Haller, Benjamin C., and Philipp W. Messer. 2019. "SLiM 3: Forward Genetic Simulations Beyond the Wright-Fisher Model." Molecular Biology and Evolution 36 (3): 632-37.
https://doi.org/10.1093/molbev/msy228
 
Kondrashov, F. A., and A. S. Kondrashov. 2001. "Multidimensional Epistasis and the Disadvantage of Sex." Proceedings of the National Academy of Sciences of the United States of America 98 (21): 12089-92.
https://doi.org/10.1073/pnas.211214298
 
Shapiro, B. Jesse, Lawrence A. David, Jonathan Friedman, and Eric J. Alm. 2009. "Looking for Darwin's Footprints in the Microbial World." Trends in Microbiology 17 (5): 196-204.
https://doi.org/10.1016/j.tim.2009.02.002 

Stritt, C., Gagneux, S. (2023). How do monomorphic bacteria evolve? The Mycobacterium tuberculosis complex and the awkward population genetics of extreme clonality. EcoEvoRxiv, ver.3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.32942/X2GW2P

How do monomorphic bacteria evolve? The *Mycobacterium tuberculosis* complex and the awkward population genetics of extreme clonalityChristoph Stritt, Sebastien Gagneux<p style="text-align: justify;">Exchange of genetic material through sexual reproduction or horizontal gene transfer is ubiquitous in nature. Among the few outliers that rarely recombine and mainly evolve by <em>de novo</em> mutation are a group o...Evolutionary Dynamics, Genome Evolution, Molecular Evolution, Population Genetics / Genomics, Reproduction and SexB. Jesse Shapiro Gonçalo Themudo2022-12-16 13:41:53 View
08 Jan 2024
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Genomic relationships among diploid and polyploid species of the genus Ludwigia L. section Jussiaea using a combination of molecular cytogenetic, morphological, and crossing investigations

Deciphering the genomic composition of tetraploid, hexaploid and decaploid Ludwigia L. species (section Jussiaea)

Recommended by based on reviews by Alex BAUMEL and Karol MARHOLD

Polyploidy, which results in the presence of more than two sets of homologous chromosomes represents a major feature of plant genomes that have undergone successive rounds of duplication followed by more or less rapid diploidization during their evolutionary history. Polyploid complexes containing diploid and derived polyploid taxa are excellent model systems for understanding the short-term consequences of whole genome duplication, and have been particularly well-explored in evolutionary ecology (Ramsey and Ramsey 2014, Rice et al. 2019). Many polyploids (especially when resulting from interspecific hybridization, i.e. allopolyploids) are successful invaders (te Beest et al. 2012) as a result of rapid genome dynamics, functional novelty, and trait evolution. The origin (parental legacy) and modes of formation of polyploids have a critical impact on the subsequent polyploid evolution. Thus, elucidation of the genomic composition of polyploids is fundamental to understanding trait evolution, and such knowledge is still lacking for many invasive species.

Genus Ludwigia is characterized by a complex taxonomy, with an underexplored evolutionary history. Species from section Jussieae form a polyploid complex with diploids, tetraploids, hexaploids, and decaploids that are notorious invaders in freshwater and riparian ecosystems (Thouvenot et al.2013).   Molecular phylogeny of the genus based on nuclear and chloroplast sequences (Liu et al. 2027) suggested some relationships between diploid and polyploid species, without fully resolving the question of the parentage of the polyploids. In their study, Barloy et al. (2023) have used a combination of molecular cytogenetics (Genomic In situ Hybridization), morphology and experimental crosses to elucidate the genomic compositions of the polyploid species, and show that the examined polyploids are of hybrid origin (allopolyploids). The tetraploid L. stolonifera derives from the diploids L. peploides subsp. montevidensis (AA genome) and L. helminthorhiza (BB genome). The tetraploid L. ascendens also share the BB genome combined with an undetermined different genome. The hexaploid L. grandiflora subsp. grandiflora has inherited the diploid AA genome combined with additional unidentified genomes. The decaploid L. grandiflora subsp. hexapetala has inherited the tetraploid L. stolonifera and the hexaploid L. grandiflora subsp. hexapetala genomes. As the authors point out, further work is needed, including additional related diploid (e.g. other subspecies of L. peploides) or tetraploid (L.  hookeri and L. peduncularis)  taxa that remain to be investigated, to address the nature of the undetermined parental genomes mentioned above. 

The presented work (Barloy et al.  2023) provides significant knowledge of this poorly investigated group with regard to genomic information and polyploid origin, and opens perspectives for future studies. The authors also detect additional diagnostic morphological traits of interest for in-situ discrimination of the taxa when monitoring invasive populations.  

References

Barloy D., Portillo-Lemus L., Krueger-Hadfield S.A., Huteau V., Coriton O. (2024). Genomic relationships among diploid and polyploid species of the genus Ludwigia L. section Jussiaea using a combination of molecular cytogenetic, morphological, and crossing investigations. BioRxiv, ver. 4 peer-reviewed and recommended  by Peer Community in Evolutionary Biology https://doi.org/10.1101/2023.01.02.522458

te Beest M., Le Roux J.J., Richardson D.M., Brysting A.K., Suda J., Kubešová M., Pyšek P. (2012). The more the better? The role of polyploidy in facilitating plant invasions. Annals of Botany, Volume 109, Issue 1 Pages 19–45, https://doi.org/10.1093/aob/mcr277

Ramsey J. and Ramsey T. S. (2014). Ecological studies of polyploidy in the 100 years following its discovery Phil. Trans. R. Soc. B369 1–20  https://doi.org/10.1098/rstb.2013.0352  

Rice, A., Šmarda, P., Novosolov, M. et al. (2019). The global biogeography of polyploid plants. Nat Ecol Evol 3, 265–273. https://doi.org/10.1038/s41559-018-0787-9

Thouvenot L, Haury J, Thiebaut G. (2013). A success story: Water primroses, aquatic plant pests. Aquat. Conserv. Mar. Freshw. Ecosyst. 23:790–803  https://doi.org/10.1002/aqc.2387  

Genomic relationships among diploid and polyploid species of the genus *Ludwigia* L. section *Jussiaea* using a combination of molecular cytogenetic, morphological, and crossing investigationsD. Barloy, L. Portillo - Lemus, S. A. Krueger-Hadfield, V. Huteau, O. Coriton<p>ABSTRACTThe genus Ludwigia L. sectionJussiaeais composed of a polyploid species complex with 2x, 4x, 6x and 10x ploidy levels, suggesting possible hybrid origins. The aim of the present study is to understand the genomic relationships among dip...Hybridization / Introgression, Phylogenetics / PhylogenomicsMalika AINOUCHE2023-01-11 13:47:18 View
29 Nov 2023
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Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations

What determines whether to scramble or fight in male bulb mites

Recommended by ORCID_LOGO based on reviews by 2 anonymous reviewers

A classic textbook example in evolutionary ecology for phenotypic plasticity—the expression of different phenotypes by a genotype under different environmental conditions—is on Daphnia (Dodson 1989). If various species of this small crustacean are exposed to predation risk or cues thereof, their offspring show induced defense phenotypes including helmets, neck teeth, or head- and tail-spines. These induced morphological changes lower the risk of being eaten by a predator. As in Daphnia, induction can span over generations, while other induced phenotypic plastic changes are almost instantaneous, including many responses in physiology and behaviour (Gabriel et al. 2005). 

Larvae male bulb mites also show plasticity in morphologies throughout development. They can develop into a costly adult fighter morphology or a less costly, but vulnerable, scrambler type. The question Deere and Smallegange (Deere & Smallegange 2023) address is whether male bulb mite larvae can anticipate which type will likely be adaptive once they become adult, or alternatively, whether the resource availability or population density they experience during their larvae phase determines frequencies of adult scrambler and fighter types. They explore this question through experimental evolution, by removing different fractions of developing intermediate larva types. They thereby manipulate the stage structure of populations and alter selective forces on these stages. The potential shift of fixed genetics, imposed by the experimental selection regimes, is evaluated by fitness assays in green garden experiments.

The exciting extension to classical experiments on phenotypic plasticity is that the authors aim at exploring eco-evolutionary feedbacks experimentally in a system that is a little more complex than basic host-parasite or predator-prey systems. The latter involve, for instance, rotifer-algae dynamics (Yoshida et al. 2003; Becks et al. 2012) or similar simple lab systems for which eco-evolutionary feedbacks have been demonstrated. The challenge for the exploration of more complex systems is revealed in the study by Deere and Smallegange. Their findings suggest that the frequencies of adult male morphotype is triggered by the environmental condition (nutrient availability) during the larval phase, i.e. a simple environmental induced plastic response. No fixed genetic shift in determining adult morphotype frequencies occurs. The trigger at the larva phase remains also not perfectly determined in their experiments, as population density and resource (food) availability are partly confounded. Additional complexity and selective aspects come into play in this system, as the targeted developmental stages that develop into fighter male morphs are also dispersal morphs. If selection on dispersal to avoid residing in food-limited environments is strong, triggering genetic shifts in fighter morphs by local population structure might be hard to experimentally achieve. Small sample sizes limit conclusions on complex interactions among duration of the experiment, population size, developmental stage types, and adult fighter frequencies. The presented study (Deere & Smallegange 2023) helps to bridge theoretical predictions and empirical evidence for eco-evolutionary feedbacks that goes beyond simple ecological-driven changes in population dynamics (Govaert et al. 2019).  

 

References

 

Becks, L., Ellner, S.P., Jones, L.E. & Hairston, N.G. (2012). The functional genomics of an eco-evolutionary feedback loop: linking gene expression, trait evolution, and community dynamics. Ecol. Lett., 15, 492-501.
https://doi.org/10.1111/j.1461-0248.2012.01763.x
 
Deere, J.A. & Smallegange, I.M. (2023). Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations. bioRxiv, 2023.02.06.527265, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology.
https://doi.org/10.1101/2023.02.06.527265
 
Dodson, S. (1989). Predator-induced Reaction Norms. Bioscience, 39, 447-452.
https://doi.org/10.2307/1311136
 
Gabriel, W., Luttbeg, B., Sih, A. & Tollrian, R. (2005). Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am. Nat., 166, 339-53.
https://doi.org/10.1086/432558
 
Govaert, L., Fronhofer, E.A., Lion, S., Eizaguirre, C., Bonte, D., Egas, M., et al. (2019). Eco-evolutionary feedbacks-Theoretical models and perspectives. Funct. Ecol., 33, 13-30.
https://doi.org/10.1111/1365-2435.13241
 
Yoshida, T., Jones, L.E., Ellner, S.P., Fussmann, G.F. & Hairston, N.G. (2003). Rapid evolution drives ecological dynamics in a predator-prey system. Nat. 2003 4246946, 424, 303-306.
https://doi.org/10.1038/nature01767

Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populationsJacques A. Deere & Isabel M. Smallegange<p style="text-align: justify;">Developmental plasticity alters phenotypes and can in that way change the response to selection. When alternative phenotypes show different life history trajectories, developmental plasticity can also affect, and be...Evolutionary Ecology, Life History, Phenotypic Plasticity, Sexual SelectionUlrich Karl Steiner2023-02-07 12:14:33 View
07 Aug 2023
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Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius erato

Impact of pollen-feeding on egg-laying and cyanogenic glucoside abundance in red postman butterflies

Recommended by based on reviews by Carol Boggs, Caroline Mueller and 1 anonymous reviewer

Growth, development and reproduction in animals are all limited by dietary nutrients. Expansion of an organism’s diet to sources not accessible to closely related species reduces food competition, and eases the constraints of nutrient-limited diets. Adult butterflies are herbivorous insects known to feed primarily on nectar from flowers, which is rich in sugars but poor in amino acids.  Only certain species in the genus Heliconius are known to also feed on pollen, which is especially rich in amino acids, and is known to prolong their lives by several months. The ability to digest pollen in Heliconius has been linked to specialized feeding behaviors (Krenn et al. 2009) and extra-oral digestion using enzymes, possibly including duplicated copies of cocoonase (Harpel et al. 2016; Smith et al. 2016 and 2018), a protease used by some moths to digest silk upon eclosion from their cocoons. In this reprint, Pinheiro de Castro and colleagues investigated the impact of artificial and natural diets on egg-laying ability, body weight, and cyanogenic glucoside abundance in adult Heliconius erato butterflies of both sexes. 

Previous studies (Dunlap-Pianka et al. 1981) in H. charithonia demonstrated that access to dietary pollen led to extended egg-laying ability among adult female butterflies compared to females deprived of pollen, and compared to Dryas iulia females which feed only on nectar. In the current study, Pinheiro de Castro et al. (2023) examine the impact of diet on both young and old H. erato, over a longer period of time than the earlier work, highlighting the importance of extending the time period over which effects are evaluated. In addition to extending egg-laying ability in older females, the authors found that pollen in the diet appeared to maintain older female body weight, presumably because the pollen contained nutrients depleted during egg-laying.

The authors then investigated the effects of nutrition on the production of cyanogenic glycoside defenses. Heliconius are aposematic butterflies that sequester cyanide-forming defense chemicals from food plants as larvae or synthesize these compounds de novo. The authors found the abundance of cyanogenic glycosides to be significantly greater in butterflies with access to pollen, but again only in older females.

Curiously, field studies of male and female H. charithonia butterflies found that females in the wild collected more pollen than males (Mendoza-Cuenca and Macías-Ordóñez 2005). Taken together, these new findings raise the intriguing possibility that females collect more pollen than males, in part, because pollen has a bigger impact on female survival and reproduction. A small limitation of the study is the use of wing length, rather than body weight, at the zero time point. But the trend is clear in both males and females, and it adds supporting detail to the efficacy of pollen feeding as an unusual strategy for increasing fertility and survival in Heliconius butterflies.

 

References
 
Dunlap-Pianka, Helen, Carol L. Boggs, Lawrence E. Gilbert. (1977) Ovarian dynamics in heliconiine butterflies: Programmed senescence versus eternal youth. Science, 197: 487-490, https://doi.org/10.1126/Science.197.4302.487
 
Pinheiro de Castro, Erika C., Josie McPherson, Glennis Julian, Anniina L. K. Mattila, Søren Bak, Stephen H. Montgomery, Chris Jiggins. (2023) Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius erato. bioRxiv, 2023.01.13.523799, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.01.13.523799
 
Krenn, Harald W., Monika J. B. Eberhard, Stefan H. Eberhard, Anna-Laetitia Hikl, Werner Huber, Lawrence E. Gilbert (2009). Mechanical damage to pollen aids nutrient acquisition in Heliconius butterflies (Nymphalidae).  Arthropod-Plant Interactions, 3: 203–208. https://doi.org/10.1007/s11829-009-9074-7
 
Harpel, Desiree, Darron A. Cullen, Swidbert R. Ott, Chris D. Jiggins, James R. Walters (2015) Pollen feeding proteomics: Salivary proteins of the passion flower butterfly, Heliconius melpomene. Insect Biochemistry and Molecular Biology, 63: 7-13, https://doi.org/10.1016/j.ibmb.2015.04.004
 
Mendoza-Cuenca, Luis, Rogelio Macías-Ordóñez (2005) Foraging polymorphism in Heliconius charitonia (Lepidoptera: Nymphalidae): morphological constraints and behavioral compensation. Journal of Tropical Ecology, 21: 407-415. https://doi.org/10.1017/S0266467405002385
 
Smith, Gilbert, Aide Macias-Muñoz, John Kelly, Carter Butts, Rachel Martin, Adriana D. Briscoe (2018) Evolutionary and structural analyses uncover a role for solvent interactions in the diversification of cocoonases in butterflies. Proceedings of the Royal Society B, 285: 20172037. https://doi.org/10.1098/rspb.2017.2037 
 
Smith, Gilbert, Aide Macias-Muñoz, Adriana D. Briscoe (2016) Gene duplication and gene expression changes play a role in the evolution of candidate pollen-feeding genes in Heliconius butterflies. Genome Biology and Evolution, 8: 2581-2596. https://doi.org/10.1093/gbe/evw180

Pollen-feeding delays reproductive senescence and maintains toxicity of Heliconius eratoErika C. Pinheiro de Castro, Josie McPherson, Glennis Jullian, Anniina L. K. Mattila, Søren Bak, Stephen Montgomery, Chris Jiggins<p>Dietary shifts may act to ease energetic constraints and allow organisms to optimise life-history traits. Heliconius butterflies differ from other nectar-feeders due to their unique ability to digest pollen, which provides a reliable source of ...Evolutionary Ecology, Life HistoryAdriana Briscoe2023-02-07 12:59:54 View
13 Nov 2023
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Color polymorphism and conspicuousness do not increase speciation rates in Lacertids

Colour polymorphism does not increase diversification rates in lizards

Recommended by based on reviews by 2 anonymous reviewers

The striking differences in species richness among lineages in the Tree of Life have long attracted much research interest. In particular, researchers have asked whether certain traits are associated with greater diversification, with a particular focus on traits under sexual selection given their direct link to mating isolation.

Polymorphism, defined as the presence of co-occurring, heritable morphs within a population, has been proposed to influence diversification rates although the effect has been proposed as both promoting or alternatively impeding speciation. The effect of polymorphism may be positive, that is facilitating speciation if polymorphism allows to broaden the ecological niche, thus enabling range expansion, or enabling maintenance of populations in variable environments. Specialized ectomorphs have been observed in several species (e.g. Kusche et al. 2015, Lattanzio and Miles 2016, Whitney et al. 2018, Scali et al. 2016). Polymorphism may also facilitate speciation if a morph is lost during the colonization of a novel area or niche, resulting in rapid divergence of the remaining morphs and reproductive isolation from the ancestral population, known as the morph speciation hypothesis (West-Eberhard 1986, Corl et al. 2010). On the other hand, polymorphism may hamper speciation through disassortative maintaining by morph, which may maintain the polymorphism through the speciation process (Jamie and Meier 2020). An example of such a process is Heliconius numata where disassortative mate preferences based on color hampers ecological speciation (Chouteau et al. 2017). Previous evidence in birds and lizards suggests polymorphism favors diversification (Corl et al. 2010b, 2012, Hugall and Stuart-Fox 2012, Brock et al. 2021).

Here, de Solan et al. (2023) test the effect of polymorphism on diversification in Lacertidae, a family of lizards containing more than 300 species distributed across Europe, Africa and Asia. The group offers a good model system to test the effect of polymorphism on speciation as it contains several species with colour polymorphism, sometimes present in both sexes but restricted to males when present in the flank. Using coloration data from the literature as well as photographs of live specimens for 295 species the authors tested whether the presence of polymorphism is associated with higher diversification rates.

While undertaking their project, another group independently tackled the same question (Brock et al. 2021), using the same model system but coming to very different conclusions. Therefore, de Solan et al. (2023) decided to also contrast their results with those of Brock et al. (2021) to determine the factors responsible for the contrasting results of both studies. The latter I consider one of the strengths of the work, given the careful re-analyses to determine the causes of the discrepancies between both studies. De Solan et al. (2023) found no association between the presence of polymorphism and diversification rates, even though they used different analytical approaches. Thus, this study is interesting as it provides results that do not support a positive effect of polymorphism on species richness. The use of a phylogeny with more limited species sampling (García-Porta et al. 2019) implied that the authors had to manually add 75 species, of which 17 were added to the tree based on information from previously published trees and 68 were added at random locations within the genus. To control for potential biases the authors repeated the analyses using a sample of trees with the imputed taxa, results were broadly concordant across the set of trees. The careful re-analysis contrasting Brock et al. (2021) and de Solan et al. (2023) results suggests the difference is mainly due to a difference in how species were coded as presenting polymorphism, which differed between the two studies, as well as a difference in the package version used to run the state-dependent diversification models. Interestingly non-parametric analyses yielded similar results across both datasets. 
 
References
 
Brock, K.M., McTavish, E.J., Edwards, D.L. 2021. Colour polymorphism is a driver of diversification in the lizard family Lacertidae. Systematic Biology. 71: 24-39. https://doi.org/10.1093/sysbio/syab046
 
Chouteau, M., Llaurens, V., Piron-Prunier, F., Joron, M. 2017. Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures. Proceedings of the National Academy of Sciences. 114: 8325-8329. https://doi.org/10.1073/pnas.1702482114
 
Corl, A., Davis, A.R., Kuchta, S.R., Comendant, T., Sinervo, B. 2010a. Alternative mating strategies and the evolution of sexual dimorphism in the side-blotched lizard, Uta stansburiana: a population-level comparative analysis. Evolution. 64: 79-96. https://doi.org/10.1111/j.1558-5646.2009.00791.x 
 
Corl, A., Davis, A.R., Kuchta, S.R., Sinervo, B. 2010b. Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation. Proceedings of the National Academy of Sciences. 107: 4254-4259. https://doi.org/10.1073/pnas.0909480107
 
Corl, A., Lancaster, L.T., Sinervo, B. 2012. Rapid formation of reproductive isolation between two populations of side-blotched lizards, Uta stansburiana. Copeia. 2012: 593-602. https://doi.org/10.1643/CH-11-166

Garcia-Porta, J., Irisarri, I., Kirchner, M. et al. 2019. Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nature Communications. 10: 4077. https://doi.org/10.1038/s41467-019-11943-x
 
Hugall, A.F., Stuart-Fox, D. 2012. Accelerated speciation in colour-polymorphic birds. Nature. 485: 631-634. https://doi.org/10.1038/nature11050
 
Jamie, G.A. and Meier, J.I. 2020. The persistence of polymorphisms across species radiations. Trends in Ecology and Evolution. 35: 795-808. https://doi.org/10.1016/j.tree.2020.04.007
 
Kusche, H., Elmer, K.R., Meyer, A. 2015. Sympatric ecological divergence associated with a colour polymorphism. BMC Biology, 13: 82. https://doi.org/10.1186/s12915-015-0192-7
 
Lattanzio, M.S. and Miles, D.B. 2016. Trophic niche divergence among colour morphs that exhibit alternative mating tactics. Royal Society Open Science. 3: 150531. https://doi.org/10.1098/rsos.150531
 
Scali, S., Sacchi, R., Mangiacotti, M., Pupin, F., Gentilli, A., Zucchi, C. Scannolo, M., Pavesi, M., Zuffi, M.A.L. 2016. Does a polymorphic species have a ‘polymorphic’ diet? A case study from a lacertid lizard. Biologcial Journal of the Linnean Society. 117: 492-502. https://doi.org/10.1111/bij.12652

de Solan T, Sinervo B, Geniez P, David P, Crochet P-A (2023) Colour polymorphism and conspicuousness do not increase speciation rates in Lacertids. bioRxiv, 2023.02.15.528678, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.02.15.528678

West-Eberhard, M.J. 1986. Alternative adaptations, speciation, and phylogeny (A review). Proceedings of the National Academy of Sciences. 83: 1388-1392. https://doi.org/10.1073/pnas.83.5.1388
 
Whitney, J.L., Donahue, M.J., Karl, S.A. 2018. Niche divergence along a fine-scale ecological gradient in sympatric colour morphs of a coral reef fish. Ecosphere. 9: e02015. https://doi.org/10.1002/ecs2.2015

Color polymorphism and conspicuousness do not increase speciation rates in LacertidsThomas de Solan, Barry Sinervo, Philippe Geniez, Patrice David, Pierre-André Crochet<p style="text-align: justify;">Conspicuous body colors and color polymorphism have been hypothesized to increase rates of speciation. Conspicuous colors are evolutionary labile, and often involved in intraspecific sexual signaling and thus may pr...Evolutionary Ecology, Macroevolution, SpeciationAlejandro Gonzalez Voyer2023-02-22 10:05:03 View
16 May 2023
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A new and almost perfectly accurate approximation of the eigenvalue effective population size of a dioecious population: comparisons with other estimates and detailed proofs

All you ever wanted to know about Ne in one handy place

Recommended by based on reviews by Jesse ("Jay") Taylor and 1 anonymous reviewer

​Of the four evolutionary forces, three can be straightforwardly summarized both conceptually and mathematically in the context of an allele at a genomic locus.  Mutation (the mutation rate, μ) is simply captured by the per-site, per-generation probability that an allele mutates into a different allele. Recombination (the recombination rate, r) is captured as the probability of recombination between two sites, wherein alleles that are in different genomes in one generation come together in the same genome in the next generation.  Natural selection (the selection coefficient, s) is captured by the probability that an allele is present in the next generation, relative to some reference.  

Random genetic drift – the random fluctuation in allele frequency due to sampling in a finite population - is not so straightforwardly summarized.  The first, and most common way of characterizing evolutionary dynamics in a finite population is the Wright-Fisher model, in which the only deviation from the assumptions of Hardy-Weinberg conditions is finite population size.  Importantly, in a W-F population, mating between diploid individuals is random, which implies self-fertile monoecy, and generations are non-overlapping.  In an ideal W-F population, the probability that a gene copy leaves i descendants in the next generation is the result of binomial sampling of uniting gametes (if the locus is biallelic).  The – and the next word is meaningful – magnitude/strength/rate/power/amount of genetic drift is proportional to 1/2N, where N is the size of the population.  All of the following are affected by genetic drift: (1) the probability that a neutral allele ultimately reaches fixation, (2) the rate of loss of genetic variation within a population, (3) the rate of increase of genetic variance among populations, (4) the amount of genetic variation segregating in a population, (5) the probability of fixation/loss of a weakly selected variant.    

Presumably no real population adheres to ideal W-F conditions, which leads to the notion of "effective population size", Ne (Wright 1931), loosely defined as "the size of an ideal W-F population that experiences an equivalent strength of genetic drift".  Almost always, Ne<N, and any violation of W-F assumptions can affect Ne.  Importantly, Ne can be defined in different ways, and the specific formulation of Ne can have different implications for evolution.  Ne was initially defined in terms of the rate of decrease of heterozygosity (inbreeding effective size) and increase in variance among populations (variance effective size).  Ewens (1979) defined the Eigenvalue effective size (equivalent to the "random extinction" effective size) and elaborated on the conditions under which the various formulations of Ne differ (Ewens 1982).  Nordborg and Krone (2002) defined the effective size in terms of the coalescent, and they identified conditions in which genetic drift cannot be described in terms of a W-F model (Sjodin et al. 2005); also see Karasov et al. (2010); Neher and Shraiman (2011).

Distinct from the issue of defining Ne is the issue of calculating Ne from data, which is the focus of this paper by De Meeus and Noûs (2023).  Pudovkin et al. (1996) showed that the Eigenvalue effective size in a dioecious population can be formulated in terms of excess heterozygosity, which the current authors note is equivalent to formulating Ne in terms of Wright's FIS statistic.  As emphasized by the title, the marquee contribution of this paper is to provide a better approximation of the Eigenvalue effective size in a dioecious population.  Science marches onward, although the empirical utility of this advance is obviously limited, given the tremendous inherent sources of uncertainty in real-world estimates of Ne.  Perhaps more valuable, however, is the extensive set of appendixes, in which detailed derivations are provided for the various formulations of effective size.  By way of analogy, the material presented here can be thought of as an extension of the material presented in section 7.6 of Crow and Kimura (1970), in which the Inbreeding and Variance effective population sizes are derived and compared.  The appendixes should serve as a handy go-to source of detailed theoretical information with respect to the different formulations of effective population size.

REFERENCES

Crow, J. F. and M. Kimura. 1970. An Introduction to Population Genetics Theory. The Blackburn Press, Caldwell, NJ.

De Meeûs, T. and Noûs, C. 2023. A new and almost perfectly accurate approximation of the eigenvalue effective population size of a dioecious population: comparisons with other estimates and detailed proofs. Zenodo, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.5281/zenodo.7927968

Ewens, W. J. 1979. Mathematical Population Genetics. Springer-Verlag, Berlin.

Ewens, W. J. 1982. On the concept of the effective population size. Theoretical Population Biology 21:373-378. https://doi.org/10.1016/0040-5809(82)90024-7

Karasov, T., P. W. Messer, and D. A. Petrov. 2010. Evidence that adaptation in Drosophila Is not limited by mutation at single sites. Plos Genetics 6. https://doi.org/10.1371/journal.pgen.1000924

Neher, R. A. and B. I. Shraiman. 2011. Genetic Draft and Quasi-Neutrality in Large Facultatively Sexual Populations. Genetics 188:975-U370. https://doi.org/10.1534/genetics.111.128876

Nordborg, M. and S. M. Krone. 2002. Separation of time scales and convergence to the coalescent in structured populations. Pp. 194–232 in M. Slatkin, and M. Veuille, eds. Modern Developments in Theoretical Population Genetics: The Legacy of Gustave Malécot. Oxford University Press, Oxford. https://www.webpages.uidaho.edu/~krone/malecot.pdf

Pudovkin, A. I., D. V. Zaykin, and D. Hedgecock. 1996. On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383-387. https://doi.org/10.1093/genetics/144.1.383

Sjodin, P., I. Kaj, S. Krone, M. Lascoux, and M. Nordborg. 2005. On the meaning and existence of an effective population size. Genetics 169:1061-1070. https://doi.org/10.1534/genetics.104.026799

Wright, S. 1931. Evolution in Mendelian populations. Genetics 16:0097-0159. https://doi.org/10.1093/genetics/16.2.97

A new and almost perfectly accurate approximation of the eigenvalue effective population size of a dioecious population: comparisons with other estimates and detailed proofsThierry de Meeûs and Camille Noûs<p>The effective population size is an important concept in population genetics. It corresponds to a measure of the speed at which genetic drift affects a given population. Moreover, this is most of the time the only kind of population size that e...Bioinformatics & Computational Biology, Evolutionary Ecology, Evolutionary Theory, Population Genetics / Genomics, Reproduction and SexCharles Baer2023-02-22 16:53:49 View
29 Nov 2023
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Does sociality affect evolutionary speed?

On the evolutionary implications of being a social animal

Recommended by based on reviews by Rafael Lucas Rodriguez and 1 anonymous reviewer

What does it mean to be highly social?  Considering the so-called four ‘pinnacles’ of animal society (Wilson, 1975) – humans, cooperative breeding as found in some non-human mammals and birds, the social insects, and colonial marine invertebrates – having inter-individual relations extending beyond the sexual pair and the parent-offspring interaction is foremost.  In many cases being social implies a high local population density, interaction with the same group of individuals over an extended time period, and an overlapping of generations.  Additional features of social species may be a wide geographical range, perhaps associated with ecological and behavioral plasticity, the latter often facilitated by cultural transmission of traditions.  

Narrowing our perspective to the domain of PCI Evolutionary Biology, we might continue our question by asking whether being social predisposes one to a special evolutionary path toward the future.  Do social species evolve faster (or slower) than their more solitary relatives such that over time they are more unlike (or similar to) those relatives (anagenesis)?  And are evolutionary changes in social species more or less likely to be accompanied by lineage splitting (cladogenesis) and ultimately speciation?  The latter question is parallel to one first posed over 40 years ago (West-Eberhard, 1979; Lande, 1981) for sexually selected traits:  Do strong mating preferences and conspicuous courtship signals generate speciation via the Fisherian process or ecological divergence?  An extensive survey of birds had found little supporting evidence (Price, 1998), but a recent one that focused on plumage complexity in tanagers did reveal a relationship, albeit a weak one (Price-Waldman et al., 2020).  Because sexual selection has been viewed as a part of the broader process of social selection (West-Eberhard, 1979), it is thus fitting to extend our surveys to the evolutionary implications of being social.

Unlike the inquiry for a sexual selection - evolutionary change connection, a social behavior counterpart has remained relatively untreated.  Diverse logistical problems might account for this oversight.  What objective proxies can be used for social behavior, and for the rate of evolutionary change within a lineage?  How many empirical studies have generated data from which appropriate proxies could be extracted?  More intractable is the conundrum arising from the connectedness between socially- and sexually-selected traits.  For example, the elevated population density found in highly social species can greatly increase the mating advantage enjoyed by an attractive male.  If anagenesis is detected, did it result from social behavior or sexual selection?  And if social behavior leads to a group structure in which male-male competition is reduced, would a modest rate of evolutionary change be support for the sexual selection - evolutionary speed connection or evidence opposing the sociality - evolution one?

Against the above odds, several biologists have begun to explore the notion that social behavior just might favor evolutionary speed in either anagenesis or cladogenesis.  In a recent analysis relying on the comparative method, Lluís Socias-Martínez and Louise Rachel Peckre (2023) combed the scientific literature archives and identified those studies with specific data on the relationships between sexual selection or social behavior and evolutionary change, either anagenesis or cladogenesis.  The authors were careful to employ fairly conservative criteria for including studies, and the number eventually retained was small.  Nonetheless, some patterns emerge:  Many more studies report anagenesis than cladogenesis, and many more report correlations with sexually-selected traits than with non-sexual social behavior ones.  And, no study indicates a potential effect of social behavior on cladogenesis.  Is this latter observation authentic or an artifact of a paucity of data?  There are some a priori reasons why cladogenesis may seldom arise.  Whereas highly social behavior could lead to fission encompassing mutually isolated population clusters within a species, social behavior may also engender counterbalancing plasticity that allows and even promotes inter-cluster migration and fusion.  And briefly – and non-systematically, as the rate of lineage splitting would need to be measured – looking at one of the pinnacles of animal social behavior, the social insects, there is little indication that diversification has been accelerated.  There are fewer than 3000 described species of termites, only ca. 16,000 ants, and the vast majority of bees and wasps are solitary.                            

Lluís Socias-Martínez and Louise Rachel Peckre provide us with a very detailed discussion of these and a myriad of other complications.  I end with a common refrain, we need more consideration of the authors’ interesting question, and much more data and analysis.  One can thank Socias-Martínez and Peckre for pointing us in that direction.

References

Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. Natn. Acad. Sci. USA 78, 3721-3725. https://doi.org/10.1073/pnas.78.6.3721

Price, T. (1998). Sexual selection and natural selection in bird speciation. Phil. Trans. Roy. Soc. B, 353, 251-260.  https://doi.org/10.1098/rstb.1998.0207  

Price‐Waldman, R. M., Shultz, A. J., & Burns, K. J. (2020). Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds. Evolution, 74(6), 1155–1169. https://doi.org/10.1111/evo.13982

Socias-Martínez and Peckre. (2023). Does sociality affect evolutionary speed? Zenodo, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.5281/zenodo.10086186

West-Eberhard, M. J. (1979). Sexual selection, social competition, and evolution. Proceedings of the American Philosophical Society, 123(4), 222–234. http://www.jstor.org/stable/2828804

Wilson, E. O. (1975). Sociobiology. The New Synthesis. Cambridge, Mass., The Belknap Press of Harvard University

Does sociality affect evolutionary speed?Lluís Socias-Martínez, Louise Rachel Peckre<p>An overlooked source of variation in evolvability resides in the social lives of animals. In trying to foster research in this direction, we offer a critical review of previous work on the link between evolutionary speed and sociality. A first ...Behavior & Social Evolution, Evolutionary Dynamics, Evolutionary Theory, Genome Evolution, Macroevolution, Molecular Evolution, Population Genetics / Genomics, Sexual Selection, SpeciationMichael D Greenfield2023-03-03 00:10:49 View
30 Oct 2023
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Telomere length vary with sex, hatching rank and year of birth in little owls, Athene noctua

Deciphering the relative contribution of environmental and biological factors driving telomere length in nestlings

Recommended by based on reviews by Florentin Remot and 1 anonymous reviewer

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

Telomere length vary with sex, hatching rank and year of birth in little owls, *Athene noctua*François Criscuolo, Inès Fache, Bertrand Scaar, Sandrine Zahn, Josefa Bleu<p>Telomeres are non-coding DNA sequences located at the end of linear chromosomes, protecting genome integrity. In numerous taxa, telomeres shorten with age and telomere length (TL) is positively correlated with longevity. Moreover, TL is also af...Evolutionary Ecology, Life HistoryJean-François Lemaitre2023-03-07 09:44:32 View