It has now been over a century since the American linguist Edward Sapir observed that there are no ‘primitive’ languages, stating ‘When it comes to linguistic form, Plato walks with the Macedonian swineherd, Confucius with the head-hunting savage of Assam’ (Sapir 1921, p. 104).  Nothing has been found among human groups since that would refute Sapir’s insight.  However, in interspecific comparisons among non-human animals, such equality is most definitely not the case, and scientists have asked what might account for some species being blessed with rich and complex communication while others seem to make do with a relatively undeveloped repertoire of signals.  Many of the investigations have focused on acoustic communications, as these are more easily identified as signals, measured, and demarcated than substrate vibrations, odors and optical displays.  But no consensus  has emerged explaining the ‘inequality among the lexicons’.

In the article ‘Colony size as the main driver of the evolution of song diversity and composition in weaverbirds’, Erwan Harscouet-Commecy and coauthors aimed to find definitive answers to the issue of interspecific differences in communication complexity.  The article considers two aspects of communication complexity, basic diversity – essentially the number of different sounds made by a species – and ‘composition’, a higher level measure centered on acoustically recognizable ‘types’ of sounds.  Sexual selection, social complexity, habitat and phylogeny are then examined as potential influences on communication.  Weaverbirds, the monophyletic family Ploceidae, including 122 species in 15 genera in sub-Saharan Africa and tropical Asia, was an eminently appropriate choice for the study.  The birds have diverse nesting and mating behavior and songs, and many have been investigated intensively.  For their analyses, the authors were quite rigorous in evaluating the species’ songs and in assessing the potential influences on song complexity.  Unexpectedly, they did not find that heightened sexual selection led to complex songs, but they note that the proxy used for sexual selection – a polygynous as opposed to a monogamous mating system – may be inaccurate.  Additionally, the strong pair bonding in monogamy may have actually selected for song complexity.  

What the authors did find was a very clear influence of social complexity, measured by colony size, and a secondary influence of phylogeny.  Questions do remain, such as the specific pathway – common genetic or common cultural heritage – along which phylogeny influences song complexity.  Another question one might raise is whether low song complexity in some species reflects reliance on other modalities of communication, e.g. plumage or movement displays.  But at present, the article appears as a gold standard for investigating the complexity of communication among animal species.    

References

Sapir, E. 1921.  Language: An Introduction to the Study of Speech.  New York: Harcourt, Brace.  ISBN 978-1-108-06378-4

E. Harscouet-Commecy, N. Adenot, A. Thetiot, N. Bresciani, D. Oschadleus, R. Covas, F. Rybak, C. Doutrelant (2024) Colony size as the main driver of the evolution of song diversity and composition in weaverbirds. OSF, ver.2 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.31219/osf.io/z5bgy_v2

The emergence and spread of insecticide resistance compromises the efficiency of insecticides as prevention tool against the transmission of insect-transmitted diseases (Moyes et al. 2017). In this context, the understanding of the genetic mechanisms of resistance and the way resistant alleles spread in insect populations is necessary and important to envision resistance management policies. A common and important mechanism of insecticide resistance is gene amplification and in particular amplification of insecticide detoxification genes, which leads to the overexpression of these genes (Bass & Field, 2011). Cattel and coauthors (2020) adopt a combination of experimental approaches to study the role of gene amplification in resistance to organophosphate insecticides in the mosquito Aedes aegypti and its occurrence in populations of South East Asia and to develop a molecular test to track resistance alleles.
Their first approach consists in performing an artificial selection on laboratory Ae. Aegypti populations started with individuals collected in Laos. In the selected population, an initial 90% mortality by adult exposure to the organophosphate insecticide malathion is imposed. This population shows a steep increase in resistance to malathion and other organophosphate insecticides, which is absent in the paired control population. The transcriptomic patterns of the control and the evolved populations as well as of a reference sensitive population reveals, among other differences, the over-expression of five carboxy/choline esterase (CCE) genes in the insecticide selected population. These five genes happen to be clustered in the Ae. aegypti genome and whole genome sequencing of a highly resistant population combined to qPCR test on genomic DNA showed that the overexpression of these genes is due to gene amplification. Although it would have been more elegant to have replicate selected and control populations and to perform the transcriptomic and the genomic analyses directly on the experimental populations, the authors gather a set of experimental evidence which combined to previous knowledge on the function of the amplified and over-expressed genes and on their implication in organophosphate insecticide resistance in other species allow to discard the possibility that this gene amplification spread by drift in the selected population.
In a second part of the paper, copy number variation for CCE genes is checked in field sample populations. This test reveals the presence of resistance alleles in half of the fourteen South East Asia populations sampled. Very interestingly, it also reveals a high level of complexity and diversity among the resistance alleles: it shows first the existence, both in the experimental and the field populations, of at least two amplified alleles (differing by the number of genes amplified) and second a high variation in the copy number of amplified genes. This indicates that gene amplification as a molecular resistance mechanism has actually lead to a high diversity of resistance alleles. These alleles are likely to differ both by the level of resistance conferred and the fitness cost imposed in the absence of the insecticide and these two values are affecting the evolution of their frequency in the field and ultimately the spread of resistance.
The last part of the paper is devoted to the development of a high-throughput Taqman assay which allows to determine rapidly the copy number of one of the esterase genes amplified in the resistance alleles described earlier. This assay is nicely validated and will definitely be a useful tool to determine the occurrence of these resistance alleles in field population. The fact that it gives access to the copy number will also allow to follow its copy number across time and get insight into the complexity of resistance evolution by gene amplification.
To sum up, this paper studies the implication of carboxy/choline esterase genes amplification in organophosphate resistance evolution in Ae. aegypti, reveals the diversity among individuals and populations of this resistance mechanism, because of variation both in the identity of the genes amplified and in their copy number and sets up a fast and efficient tool to detect and follow the spread of these resistant alleles in the field. Additionally, the different experimental approaches adopted have generated genomic and transcriptomic data, of which only the part related to CCE gene amplification has been exploited. These data are very likely to reveal other genomic and expression determinants of resistance that will give access to an extra degree of complexity in organophosphate insecticide resistance determinism and evolution.

References

Bass C, Field LM (2011) Gene amplification and insecticide resistance. Pest Management Science, 67, 886–890. https://doi.org/10.1002/ps.2189
Cattel J, Haberkorn C, Laporte F, Gaude T, Cumer T, Renaud J, Sutherland IW, Hertz JC, Bonneville J-M, Arnaud V, Nous C, Fustec B, Boyer S, Marcombe S, David J-P (2020) A genomic amplification affecting a carboxylesterase gene cluster confers organophosphate resistance in the mosquito Aedes aegypti: from genomic characterization to high-throughput field detection. bioRxiv, 2020.06.08.139741, ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. https://doi.org/10.1101/2020.06.08.139741
Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, Raghavendra K, Pinto J, Corbel V, David J-P, Weetman D (2017) Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLOS Neglected Tropical Diseases, 11, e0005625. https://doi.org/10.1371/journal.pntd.0005625

Several examples of chromosomal inversions carrying genes affecting mate choice have been reported from various organisms. Furthermore, inversions are also frequently involved in genetic isolation between populations or species. Past work has shown that inversions can spread when they capture not only some loci involved in mate choice but also loci involved in incompatibilities between hybridizing populations [1]. In this new paper [2], the authors derive analytical approximations for the selection coefficient associated with an inversion suppressing recombination between a locus involved in mate choice and one (or several) locus involved in Dobzhansky-Muller incompatibilities. Two mechanisms for mate choice are considered: assortative mating based on the allele present at a single locus, or a trait-preference model where one locus codes for the trait and another for the preference. The results show that such an inversion is generally favoured, the selective advantage associated with the inversion being strongest when hybridization is sufficiently frequent. Assuming pairwise epistatic interactions between loci involved in incompatibilities, selection for the inversion increases approximately linearly with the number of such loci captured by the inversion.

This paper is a good read for several reasons. First, it presents the problem clearly (e.g. the introduction provides a clear and concise presentation of the issue and past work) and its crystal-clear writing facilitates the reader's understanding of theoretical approaches and results. Second, the analysis is competently done and adds to previous work by showing that very general conditions are expected to be favourable to the spread of the type of inversion considered here. And third, it provides food for thought about the role of inversions in the origin or the reinforcement of divergence between nascent species. One result of this work is that an inversion linked to pre-zygotic isolation "is favoured so long as there is viability selection against recombinant genotypes", suggesting that genetic incompatibilities must have evolved first and that inversions capturing mating preference loci may then enhance pre-existing reproductive isolation. However, the results also show that inversions are more likely to be favoured in hybridizing populations among which gene flow is still high, rather than in more strongly isolated populations. This matches the observation that inversions are more frequently observed between sympatric species than between allopatric ones.

References

[1] Trickett AJ, Butlin RK. 1994. Recombination Suppressors and the Evolution of New Species. Heredity 73:339-345. doi: 10.1038/hdy.1994.180

[2] Dagilis AJ, Kirkpatrick M. 2016. Prezygotic isolation, mating preferences, and the evolution of chromosomal inversions. Evolution 70: 1465–1472. doi: 10.1111/evo.12954

Genome-wide data obtained from even a small number of individuals can provide unprecedented levels of detail about the evolutionary history of populations and species [1], determinants of genetic diversity [2], species boundaries and the process of speciation itself [3]. Loire and Galtier [4] present a clear example, using the emblematic Galápagos giant tortoise (Chelonoidis nigra), of how multi-species comparative population genomic approaches can provide valuable insights about population structure and species delimitation even when sample sizes are limited but the number of loci is large and distributed across the genome.

Galápagos giant tortoises are endemic to the Galápagos Islands and are currently recognized as an endangered, multi-species complex including both extant and extinct taxa. Taxonomic definitions are based on morphology, geographic isolation and population genetic evidence based on short DNA sequences of the mitochondrial genome (mtDNA) and/or a dozen or so nuclear microsatellite loci [5-8]. The species complex enjoys maximal protection. Population recoveries have been quite successful and spectacular conservation programs based on mitochondrial genes and microsatellites are ongoing. This includes for example individual translocations, breeding program, “hybrid” sterilization or removal, and resurrection of extinct lineages).

In 2013, Loire et al. [9] provided the first population genomic analyses based on genome scale data (~1000 coding loci derived from blood-transcriptomes) from five individuals, encompassing three putative “species”: Chelonnoidis becki, C. porteri and C. vandenburghi. Their results raised doubts about the validity/accuracy of the currently accepted designations of “genetic distinctiveness”. However, the implications for conservation and management have remained unnoticed.

In 2017, Loire and Galtier [4] have re-appraised this issue using an original multi-species comparative population genomic analysis of their previous data set [9]. Based on a comparison of 53 animal species, they show that both the level of genome-wide neutral diversity (πS) and level of population structure estimated using the inbreeding coefficient (F) are much lower than would be expected from a sample covering multiple species. The observed values are more comparable to those typically reported at the “among population” level within a single species such as human (Homo sapiens). The authors go to great length to assess the sensitivity of their method to detect population structure (or lack thereof) and show that their results are robust to potential issues, such as contamination and sequencing errors that can occur with Next Generation Sequencing techniques; and biases related to the small sample size and sub-sampling of individuals. They conclude that published mtDNA and microsatellite-based assessment of population structure and species designations may be biased towards over-splitting.

This manuscript is a very good read as it shows the potential of the now relatively affordable genome-wide data for helping to both resolve and clarify population and species boundaries, illuminate demographic trends, evolutionary trajectories of isolated groups, patterns of connectivity among them, and test for evidence of local adaptation and even reproductive isolation. The comprehensive information provided by genome-wide data can critically inform and assist the development of the best strategies to preserve endangered populations and species. Loire and Galtier [4] make a strong case for applying genomic data to the Galápagos giant tortoises, which is likely to redirect conservation efforts more effectively and at lower cost. The case of the Galápagos giant tortoises is certainly a very emblematic example, which will find an echo in many other endangered species conservation programs.

References

[1] Li H and Durbin R. 2011. Inference of human population history from individual whole-genome sequences. Nature, 475: 493–496. doi: 10.1038/nature10231

[2] Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V, Chenuil A, Chiari Y, Dernat R, Duret L, Faivre N, Loire E, Lourenco JM, Nabholz B, Roux C, Tsagkogeorga G, Weber AA-T, Weinert LA, Belkhir K, Bierne N, Glémin S and Galtier N. 2014. Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515: 261–263. doi: 10.1038/nature13685

[3] Roux C, Fraïsse C, Romiguier J, Anciaux Y, Galtier N and Bierne N. 2016. Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology, 14: e2000234. doi: 10.1371/journal.pbio.2000234

[4] Loire E and Galtier N. 2017. Lacking conservation genomics in the giant Galápagos tortoise. bioRxiv 101980, ver. 4 of September 26, 2017. doi: 10.1101/101980

[5] Beheregaray LB, Ciofi C, Caccone A, Gibbs JP and Powell JR. 2003. Genetic divergence, phylogeography and conservation units of giant tortoises from Santa Cruz and Pinzón, Galápagos Islands. Conservation Genetics, 4: 31–46. doi: 10.1023/A:1021864214375

[6] Ciofi C, Milinkovitch MC, Gibbs JP, Caccone A and Powell JR. 2002. Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises. Molecular Ecology, 11: 2265–2283. doi: 10.1046/j.1365-294X.2002.01617.x

[7] Garrick RC, Kajdacsi B, Russello MA, Benavides E, Hyseni C, Gibbs JP, Tapia W and Caccone A. 2015. Naturally rare versus newly rare: demographic inferences on two timescales inform conservation of Galápagos giant tortoises. Ecology and Evolution, 5: 676–694. doi: 10.1002/ece3.1388

[8] Poulakakis N, Edwards DL, Chiari Y, Garrick RC, Russello MA, Benavides E, Watkins-Colwell GJ, Glaberman S, Tapia W, Gibbs JP, Cayot LJ and Caccone A. 2015. Description of a new Galápagos giant tortoise species (Chelonoidis; Testudines: Testudinidae) from Cerro Fatal on Santa Cruz island. PLoS ONE, 10: e0138779. doi: 10.1371/journal.pone.0138779

[9] Loire E, Chiari Y, Bernard A, Cahais V, Romiguier J, Nabholz B, Lourenço JM and Galtier N. 2013. Population genomics of the endangered giant Galápagos tortoise. Genome Biology, 14: R136. doi: 10.1186/gb-2013-14-12-r136

Much research effort has been extended toward developing systems for managing soil inhabiting insect pests of crops with entomopathogenic nematodes as biocontrol agents. Although small plot or laboratory experiments may suggest a particular insect pest is vulnerable to management in this way, it is often difficult to scale-up nematode production for application at the field- and farm scale to make such a tactic viable. Part of the problem is that entomopathogenic nematode strains must be propagated by serial passage in vivo, because storage by freezing decreases fitness. At the same time, serial propagation results in loss of virulence (ability to infect) over generations in the laboratory, a phenomenon called attenuation.

To probe the underlying reasons for development of attenuation, as a prerequisite to designing strategies to mitigate it, Shapiro-Ilan and Raymond [1] turned to evolutionary theory of social conflict as a possible explanatory framework. Virulence of entomopathogenic nematodes depends on a combination of virulence factors, like various proteases, secreted by both the nematode and symbiotic bacteria to overcome host defenses. Attenuation is characterized in part by a reduced production of these factors. Invasion of a host involves simultaneous attack by a group of nematodes ("cooperators"), which together neutralize host defenses enough to allow individuals to successfully invade. "Cheaters" in the invading population can avoid the metabolic costs of producing virulence factors while reaping the benefits of infecting the host made vulnerable by the cooperators in the population. The authors hypothesize that an increase in frequency of cheaters may contribute to attenuation of virulence during serial propagation in the laboratory. The evolutionary dynamics of cheater frequency in a population have been explored in many contexts as part of kin selection theory. Cheaters can increase in a population by outcompeting cooperators in a host if overall relatedness within the invading population is low. Conversely, frequency of altruism, or costly cooperation, increases in a population if relatedness is high, which is enhanced by low effective dispersal. However, a population that is too isolated can suffer from inbreeding effects, and competition will occur mainly among relatives, which decreases the fitness benefits of altruism.

Shapiro-Ilan and Raymond [1] tested changes in virulence and reproductive output in a serially propagated entomopathogenic nematode, Heterorhabditis floridensis. They compared lines of high or low relatedness, manipulated via multiplicity of infection (MOI) rates (where a low dose of nematodes gives high relatedness and a high dose gives low relatedness); and under global or local competition, manipulated by pooling populations emerging from all or only two host cadavers per generation, respectively. As predicted, treatments of high relatedness (low MOI) and global competition had the greatest level of reproduction, while all lines of low relatedness (high MOI) evolved decreased reproduction and decreased virulence, which led to extinction. The key finding was that lines in the high relatedness (low MOI) and low (local) competition treatment exhibited the most stable virulence through the 12 generations tested. Thus, to minimize attenuation of virulence while maintaining fitness of recently isolated entomopathogenic nematodes, the authors recommend insect hosts be inoculated with low doses of nematodes from inocula pools from as few cadavers as possible.

The application of evolutionary theory, with a clever experimental design, to an important problem in pest management makes this paper particularly noteworthy.

Reference

[1] Shapiro-Ilan D, Raymond B. 2016. Limiting opportunities for cheating stabilizes virulence in insect parasitic nematodes. Evolutionary Applications 9:462-470. doi: 10.1111/eva.12348