Adaptations to a new ecological niche allow species to access new resources and circumvent competitors and are hence obvious pathways of evolutionary success. The evolution of agricultural pest species represents an important case to study how a species adapts, on various timescales, to a novel ecological niche. Among the numerous insects that are agricultural pests, the ability to lay eggs (or oviposit) in ripe fruit appears to be a recurrent scenario. Fruit flies (family Tephritidae) employ this strategy, and include amongst their members some of the most destructive pests (e.g., the olive fruit fly Bactrocera olea or the medfly Ceratitis capitata). In their ms, Karageorgi et al. [1] studied how Drosophila suzukii, a new major agricultural pest species that recently invaded Europe and North America, evolved the novel behavior of laying eggs into undamaged fresh fruit. The close relatives of D. suzukii lay their eggs on decaying plant substrates, and thus this represents a marked change in host use that links to substantial economic losses to the fruit industry. Although a handful of studies have identified genetic changes causing new behaviors in various species, the question of the evolution of behavior remains a largely uncharted territory. The study by Karageorgi et al. [1] represents an original and most welcome contribution in this domain for a non-model species. Using clever behavioral experiments to compare D. suzukii to several related Drosophila species, and complementing those results with neurogenetics and mutant analyses using D. suzukii, the authors nicely dissect the sensory changes at the origin of the new egg-laying behavior. The experiments they describe are easy to follow, richly illustrate through figures and images, and particularly well designed to progressively decipher the sensory bases driving oviposition of D. suzukii on ripe fruit. Altogether, Karageorgi et al.’s [1] results show that the egg-laying substrate preference of D. suzukii has considerably evolved in concert with its morphology (especially its enlarged, serrated ovipositor that enables females to pierce the skin of many ripe fruits). Their observations clearly support the view that the evolution of traits that make D. suzukii an agricultural pest included the modification of several sensory systems (i.e. mechanosensation, gustation and olfaction). These differences between D. suzukii and its close relatives collectively underlie a radical change in oviposition behavior, and were presumably instrumental in the expansion of the ecological niche of the species. The authors tentatively propose a multi-step evolutionary scenario from their results with the emergence of D. suzukii as a pest species as final outcome. Such formalization represents an interesting evolutionary model-framework that obviously would rely upon further data and experiments to confirm and refine some of the evolutionary steps proposed, especially the final and recent transition of D. suzukii from non-invasive to invasive species.

References

[1] Karageorgi M, Bräcker LB, Lebreton S, Minervino C, Cavey M, Siju KP, Grunwald Kadow IC, Gompel N, Prud’homme B. 2017. Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukii. Current Biology, 27: 1-7. doi: 10.1016/j.cub.2017.01.055

150 years after Darwin published ‘Descent of man and selection in relation to sex’ (Darwin, 1871), the evolutionary mechanism that he laid out in his treatise continues to fascinate us. Sexual selection is responsible for some of the most spectacular traits among animals, and plants, and it appeals to our interest in all things reproductive and sexual (Bell, 1982). In addition, sexual selection poses some of the more intractable problems in evolutionary biology: Its realm encompasses traits that are subject to markedly different selection pressures, particularly when distinct, yet associated, traits tend to be associated with males, e.g. courtship signals, and with females, e.g. preferences (cf. Ah-King & Ahnesjo, 2013). While separate, such traits cannot evolve independently of each other (Arnqvist & Rowe, 2005), and complex feedback loops and correlations between them are predicted (Greenfield et al., 2014). Traditionally, sexual selection has been modelled under simplifying assumptions, and quantitative genetic approaches that avoided evolutionary dynamics have prevailed. New computing methods may be able to free the field from these constraints, and a trio of theoreticians (Chevalier, De Coligny & Labonne 2020) describe here a novel application of a ‘demo-genetic agent (or individual) based model’, a mouthful hereafter termed DG-ABM, for arriving at a holistic picture of the sexual selection trajectory. The application is built on the premise that traits, e.g. courtship, preference, gamete investment, competitiveness for mates, can influence the genetic architecture, e.g. correlations, of those traits. In turn, the genetic architecture can influence the expression and evolvability of the traits. Much of this influence occurs via demographic features, i.e. social environment, generated by behavioral interactions during sexual advertisement, courtship, mate guarding, parental care, post-mating dispersal, etc.
The authors provide a lengthy verbal description of their model, specifying the genomic and behavioral parameters that can be set and how a ‘run’ may be initialized. There is a link to an internet site where users can then enter their own parameter values and begin exploring hypotheses. Back in the article several simulations illustrate simple tests; e.g. how gamete investment and preference jointly evolve given certain survival costs. One obvious test would have been the preference – courtship genetic correlation that represents the core of Fisherian runaway selection, and it is regrettable that it was not examined under a range of demographic parameters. As presented the author’s DG-ABM appears particularly geared toward mating systems in ‘higher’ vertebrates, where couples form during a discrete mating season and are responsible for most reproduction. It is not clear how applicable the model could be to a full range of mating systems and nuances, including those in arthropods and other invertebrates as well as plants.
What is the likely value of the DG-ABM for sexual selection researchers? We will not be able to evaluate its potential impact until readers with specialized understanding of a question and taxon begin exploring and comparing their results with prior expectations. Of course, lack of congruence with earlier predictions would not invalidate the model. Hopefully, some of these specialists will have opportunities for comparing results with pertinent empirical data.

References

Ah-King, M. and Ahnesjo, I. 2013. The ‘sex role’ concept: An overview and evaluation Evolutionary Biology, 40, 461-470. doi: https://doi.org/10.1007/s11692-013-9226-7
Arnqvist, G. and Rowe, L. 2005. Sexual Conflict. Princeton University Press, Princeton. doi: https://doi.org/10.1515/9781400850600
Bell, G. 1982. The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley.
Chevalier, L., De Coligny, F. and Labonne, J. (2020) A demogenetic individual based model for the evolution of traits and genome architecture under sexual selection. bioRxiv, 2020.04.01.014514, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: https://doi.org/10.1101/2020.04.01.014514
Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. J. Murray, London.
Greenfield, M.D., Alem, S., Limousin, D. and Bailey, N.W. 2014. The dilemma of Fisherian sexual selection: Mate choice for indirect benefits despite rarity and overall weakness of trait-preference genetic correlation. Evolution, 68, 3524-3536. doi: https://doi.org/10.1111/evo.12542

Explaining long periods of evolutionary stasis, the absence of change in trait means over geological times, despite the existence of abundant genetic variation in most traits has challenged evolutionary theory since Darwin's theory of evolution by gradual modification (Estes & Arnold 2007). Stasis observed in contemporary populations is even more daunting since ample genetic variation is usually coupled with the detection of selection differentials (Kruuk et al. 2002, Morrissey et al. 2010). Moreover, rapid adaptation to environmental changes in contemporary populations, fuelled by standing genetic variation provides evidence that populations can quickly respond to an adaptive challenge. Explanations for evolutionary stasis usually invoke stabilizing selection as a main actor, whereby optimal trait values remain roughly constant over long periods of time despite small-scale environmental fluctuations. Genetic correlation among traits may also play a significant role in constraining evolutionary changes over long timescales (Schluter 1996). Yet, genetic constraints are rarely so strong as to completely annihilate genetic changes, and they may evolve. Patterns of genetic correlations among traits, as captured in estimates of the G-matrix of additive genetic co-variation, are subject to changes over generations under the action of drift, migration, or selection, among other causes (Arnold et al. 2008). Therefore, under the assumption of stabilizing selection on a set of traits, phenotypic stasis and genetic divergence in patterns of trait correlations may both be observed when selection on trait correlations is weak relative to its effect on trait means.

Mallard et al. (2023) set out to test whether selection or drift may explain the divergence in genetic correlation among traits in experimental lines of the nematode Caenorhabditis elegans and whether stabilizing selection may be a driver of phenotypic stasis. To do so, they analyzed the evolution of locomotion behavior traits over 100 generations of lab evolution in a constant and homogeneous environment after 140 generations of domestication from a largely differentiated set of founder populations. The locomotion traits were transition rates between movement states and direction (still, forward or backward movement). They could estimate the traits' broad-sense G-matrix in three populations at two generations (50 and 100), and in the ancestral mixed population. Similarly, they estimated the shape of the selection surface by regressing locomotion behavior on fertility. Armed with both G-matrix and surface estimates, they could test whether the G's orientation matched selection's orientation and whether changes in G were constrained by selection. They found stasis in trait mean over 100 generations but divergence in the amount and orientation of the genetic variation of the traits relative to the ancestral population. The selected populations changed orientation of their G-matrices and lost genetic variation during the experiment in agreement with a model of genetic drift on quantitative traits. Their estimates of selection also point to mostly stabilizing selection on trait combinations with weak evidence of disruptive selection, suggesting a saddle-shaped selection surface. The evolutionary responses of the experimental populations were mostly consistent with small differentiation in the shape of G-matrices during the 100 generations of stabilizing selection.

Mallard et al. (2023) conclude that phenotypic stasis was maintained by stabilizing selection and drift in their experiment. They argue that their findings are consistent with a "table-top mountain" model of stabilizing selection, whereby the population is allowed some wiggle room around the trait optimum, leaving space for random fluctuations of trait variation, and especially trait co-variation. The model is an interesting solution that might explain how stasis can be maintained over contemporary times while allowing for random differentiation of trait genetic co-variation. Whether such differentiation can then lead to future evolutionary divergence once replicated populations adapt to a new environment is an interesting idea to follow.

References

Arnold, S. J., Bürger, R., Hohenlohe, P. A., Ajie, B. C. and Jones, A. G. 2008. Understanding the evolution and stability of the G-matrix. Evolution 62(10): 2451-2461. 
https://doi.org/10.1111/j.1558-5646.2008.00472.x
 
Estes, S. and Arnold, S. J. 2007. Resolving the Paradox of Stasis: Models with Stabilizing Selection Explain Evolutionary Divergence on All Timescales.. Am. Nat. 169(2): 227-244.
https://doi.org/10.1086/510633
 
Kruuk, L. E. B., Slate, J., Pemberton, J. M., Brotherstone, S., Guinness, F. and Clutton-Brock, T. 2002. Antler size in red deer: Heritability and selection but no evolution. Evolution 56(8): 1683-1695.
https://doi.org/10.1111/j.0014-3820.2002.tb01480.x
 
Mallard, F., Noble, L., Guzella, T., Afonso, B., Baer, C. F., Teotónio, H. 2023. Phenotypic stasis with genetic divergence. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology.
https://doi.org/10.1101/2022.05.28.493856
 
Morrissey, M. B., Kruuk, L. E. B. and Wilson, A. J. 2010. The danger of applying the breeder's equation in observational studies of natural populations. J Evolution Biol 23(11): 2277-2288. 
https://doi.org/10.1111/j.1420-9101.2010.02084.x
 
Schluter, D. 1996. Adaptive radiation along genetic lines of least resistance. Evolution 50(5): 1766-1774. 
https://doi.org/10.1111/j.1558-5646.1996.tb03563.x

Two back-to-back papers published earlier this year in Nature Genetics provide compelling evidence for the control of a male reproductive polymorphism in a wading bird by a "supergene", a cluster of tightly linked genes [1-2]. The bird in question, the ruff (Philomachus pugnax), has a rather unusual reproductive system that consists of three distinct types of males ("reproductive morphs"): aggressive "independents" who represent the majority of males; a smaller fraction of non-territorial "satellites" who are submissive towards "independents"; and "faeders" who mimic females and are rare. Previous work has shown that the male morphs differ in major aspects of mating and aggression behavior, plumage coloration and body size, and that – intriguingly – this complex multi-trait polymorphism is apparently controlled by a single autosomal Mendelian locus with three alleles [3]. To uncover the genetic control of this polymorphism two independent teams, led by Terry Burke [1] and Leif Andersson [2], have set out to analyze the genomes of male ruffs. Using a combination of genomics and genetics, both groups managed to pin down the supergene locus and map it to a non-recombining, 4.5 Mb large inversion which arose 3.8 million years ago. While "independents" are homozygous for the ancestral uninverted sequence, "satellites" and "faeders" carry evolutionarily divergent, dominant alternative haplotypes of the inversion. Thus, as in several other notable cases, for example the supergene control of disassortative mating, aggressiveness and plumage color in white-throated sparrows [4], of mimicry in Heliconius and Papilio butterflies [5-6], or of social structure in ants [7], an inversion – behaving as a single "locus" – underpins the mechanistic basis of the supergene. More generally, and beyond inversions, a growing number of studies now shows that selection can favor the evolution of suppressed recombination, thereby leading to the emergence of clusters of tightly linked loci which can then control – presumably due to polygenic gene action – a suite of complex phenotypes [8-10]. A largely unresolved question in this field concerns the identity of the causative alleles and loci within a given supergene. Recent progress on this question has been made for example in Papilio polytes butterflies where a mimicry supergene has been found to involve – surprisingly – only a single but large gene: multiple mimicry alleles in the doublesex gene are maintained in strong linkage disequilibrium via an inversion. It will clearly be of great interest to see future examples of such a fine-scale genetic dissection of supergenes. In conclusion, we were impressed by the data and analyses of Küpper et al. [1] and Lamichhaney et al. [2]: both papers beautifully illustrate how genomics and evolutionary ecology can be combined to make new, exciting discoveries. Both papers will appeal to readers with an interest in supergenes, inversions, the interplay of selection and recombination, or the genetic control of complex phenotypes.

References

[1] Küpper C, Stocks M, Risse JE, dos Remedios N, Farrell LL, McRae SB, Morgan TC, Karlionova N, Pinchuk P, Verkuil YI, et al. 2016. A supergene determines highly divergent male reproductive morphs in the ruff. Nature Genetics 48:79-83. doi: 10.1038/ng.3443

[2] Lamichhaney S, Fan G, Widemo F, Gunnarsson U, Thalmann DS, Hoeppner MP, Kerje S, Gustafson U, Shi C, Zhang H, et al. 2016. Structural genomic changes underlie alternative reproductive strategies in the ruff (Philomachus pugnax). Nature Genetics 48:84-88. doi: 10.1038/ng.3430

[3] Lank DB, Smith CM, Hanotte O, Burke T, Cooke F. 1995. Genetic polymorphism for alternative mating behaviour in lekking male ruff Philomachus pugnax. Nature 378:59-62. doi: 10.1038/378059a0

[4] Tuttle Elaina M, Bergland Alan O, Korody Marisa L, Brewer Michael S, Newhouse Daniel J, Minx P, Stager M, Betuel A, Cheviron Zachary A, Warren Wesley C, et al. 2016. Divergence and Functional Degradation of a Sex Chromosome-like Supergene. Current Biology 26:344-350. doi: 10.1016/j.cub.2015.11.069

[5] Joron M, Frezal L, Jones RT, Chamberlain NL, Lee SF, Haag CR, Whibley A, Becuwe M, Baxter SW, Ferguson L, et al. 2011. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477:203-206. doi: 10.1038/nature10341

[6] Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR. 2014. doublesex is a mimicry supergene. Nature 507:229-232. doi: 10.1038/nature13112

[7] Wang J, Wurm Y, Nipitwattanaphon M, Riba-Grognuz O, Huang Y-C, Shoemaker D, Keller L. 2013. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493:664-668. doi: 10.1038/nature11832

[8] Thompson MJ, Jiggins CD. 2014. Supergenes and their role in evolution. Heredity 113:1-8. doi: 10.1038/hdy.2014.20

[9] Schwander T, Libbrecht R, Keller L. 2014. Supergenes and Complex Phenotypes. Current Biology 24:R288-R294. doi: 10.1016/j.cub.2014.01.056

[10] Charlesworth D. 2015. The status of supergenes in the 21st century: recombination suppression in Batesian mimicry and sex chromosomes and other complex adaptations. Evolutionary Applications 9:74-90. doi: 10.1111/eva.12291

Many organisms across the Tree of life have the ability to produce seeds, eggs, cysts, or spores, that can remain dormant for several generations before hatching. This widespread adaptive trait in bacteria, fungi, plants and animals, has a significant impact on the ecology, population dynamics and population genetics of species that express it (Evans and Dennehy 2005).

In population genetics, and despite the recognition of its evolutionary importance in many empirical studies, few theoretical models have been developed to characterize the evolutionary consequences of this trait on the level and distribution of neutral genetic diversity (see, e.g., Kaj et al. 2001; Vitalis et al. 2004), and also on the dynamics of selected alleles (see, e.g., Živković and Tellier 2018). However, due to the complexity of the interactions between evolutionary forces in the presence of dormancy, the fate of selected mutations in their genomic environment is not yet fully understood, even from the most recently developed models.

In a comprehensive article, Korfmann et al. (2023) aim to fill this gap by investigating the effect of germ banking on the probability of (and time to) fixation of beneficial mutations, as well as on the shape of the selective sweep in their vicinity. To this end, Korfmann et al. (2023) developed and released their own forward-in-time simulator of genome-wide data, including neutral and selected polymorphisms, that makes use of Kelleher et al.’s (2018) tree sequence toolkit to keep track of gene genealogies.

The originality of Korfmann et al.’s (2023) study is to provide new quantitative results for the effect of dormancy on the time to fixation of positively selected mutations, the shape of the genomic landscape in the vicinity of these mutations, and the temporal dynamics of selective sweeps. Their major finding is the prediction that germ banking creates narrower signatures of sweeps around positively selected sites, which are detectable for increased periods of time (as compared to a standard Wright-Fisher population).

The availability of Korfmann et al.’s (2023) code will allow a wider range of parameter values to be explored, to extend their results to the particularities of the biology of many species. However, as they chose to extend the haploid coalescent model of Kaj et al. (2001), further development is needed to confirm the robustness of their results with a more realistic diploid model of seed dormancy.

REFERENCES

Evans, M. E. K., and J. J. Dennehy (2005) Germ banking: bet-hedging and variable release from egg and seed dormancy. The Quarterly Review of Biology, 80(4): 431-451. https://doi.org/10.1086/498282

Kaj, I., S. Krone, and M. Lascoux (2001) Coalescent theory for seed bank models. Journal of Applied Probability, 38(2): 285-300. https://doi.org/10.1239/jap/996986745

Kelleher, J., K. R. Thornton, J. Ashander, and P. L. Ralph (2018) Efficient pedigree recording for fast population genetics simulation. PLoS Computational Biology, 14(11): e1006581. https://doi.org/10.1371/journal.pcbi.1006581

Korfmann, K., D. Abu Awad, and A. Tellier (2023) Weak seed banks influence the signature and detectability of selective sweeps. bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.04.26.489499

Vitalis, R., S. Glémin, and I. Olivieri (2004) When genes go to sleep: the population genetic consequences of seed dormancy and monocarpic perenniality. American Naturalist, 163(2): 295-311. https://doi.org/10.1086/381041

Živković, D., and A. Tellier (2018). All but sleeping? Consequences of soil seed banks on neutral and selective diversity in plant species. Mathematical Modelling in Plant Biology, 195-212. https://doi.org/10.1007/978-3-319-99070-5_10