In this paper (Manas et al., 2023), the authors investigate male responses to risk of sperm competition in the black soldier fly Hermetia illuce, a widespread insect that has gained recent attention for its potential to be farmed for sustainable food production (Tomberlin & van Huis, 2020).

Using an experimental approach that simulated low-risk (males were kept individually) and high-risk (males were kept in groups of 10) of sperm competition, they found that males reared in groups showed a significant increase in sperm production compared with males reared individually. This shows a response to the rearing environment in sperm production that is consistent with an increase in the perceived risk of sperm competition.

These males were then used in mating experiments to determine whether sperm allocation to females during mating was influenced by the perceived risk of sperm competition. Mating experiments were initiated in groups, since mating only occurs when more than one male and one female are present, indicating strong sexual selection in the wild. Once a copulation began, the pair was moved to a new environment with no competition, with male competitors, or with other females, to test how social environment and potentially the sex of surrounding individuals influenced sperm allocation during mating. Copulation duration and the number of sperm transferred were subsequently counted.

In these mating experiments, the number of sperm stored in the female spermathecae increased under immediate risk of sperm competition. Interestingly, this was not because males copulated for longer depending on the risk of sperm competition, indicating that males respond plastically to the risk of competition by elevating their investment in sperm production and speed of sperm transfer. There was no difference between competitive environments consisting of males or females respectively, suggesting that it is the presence of other flies per se that influence sperm allocation.

The study provides an interesting new example of how males alter reproductive investment in response to social context and sexual competition in their environment. In addition, it provides new insights into the reproductive biology of the black soldier fly Hermetia illucens, which may be relevant for optimizing farming conditions.

References

Manas F, Labrousse C, Bressac C (2023) Sperm production and allocation in response to risks of sperm competition in the black soldier fly Hermetia illucens. bioRxiv, 2023.06.20.544772, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology.  https://doi.org/10.1101/2023.06.20.544772

Tomberlin JK, Van Huis A (2020) Black soldier fly from pest to ‘crown jewel’ of the insects as feed industry: an historical perspective. Journal of Insects as Food and Feed, 6, 1–4. https://doi.org/10.3920/JIFF2020.0003

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

The article “Drivers of genomic landscapes of differentiation across Populus divergence gradient” by Shang et al. describes an amazing dataset where genomic variations among 21 pairs of diverging poplar species are compared. Such comparisons are still quite rare and are needed to shed light on the processes shaping genomic divergence along the speciation gradient. Relying on two hundred whole-genome resequenced samples from 8 species that diverged from 1.3 to 4.8 million years ago, the authors aim at identifying the key factors involved in the genomic differentiation between species. They carried out a wide range of robust statistical tests aiming at characterizing the genomic differentiation along the genome of these species pairs. They highlight in particular the role of linked selection and gene flow in shaping the divergence along the genomes of species pairs. They also confirm the significance of introgression among species with a net divergence larger than the upper boundaries of the grey zone of speciation previously documented in animals (da from 0.005 to 0.02, Roux et al. 2016). Because these findings pave the way to research about the genomic mechanisms associated with speciation in species with allopatric and parapatric distributions, I warmingly recommend this article.

References

Roux C, Fraïsse C, Romiguier J, Anciaux Y, Galtier N, Bierne N (2016) Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence. PLOS Biology, 14, e2000234. https://doi.org/10.1371/journal.pbio.2000234

Shang H, Rendón-Anaya M, Paun O, Field DL, Hess J, Vogl C, Liu J, Ingvarsson PK, Lexer C, Leroy T (2023) Drivers of genomic landscapes of differentiation across Populus divergence gradient. bioRxiv, 2021.08.26.457771, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.08.26.457771

Periodical cicadas are a very prominent insect group in North America that are known for their large size, good looks, and loud sounds. However, they are probably known best to evolutionary ecologists because of their long juvenile periods of 13 or 17 years (prime numbers!), which they spend in the ground. Multiple related species living in the same area are often coordinated in emerging as adults during the same year, thereby presumably swamping any predators specialized on eating them.
Life history differences between the 13yr and 17yr cicadas are a particular focus of interest. For example, as it takes time to grow large, one would expect 17yr cicadas to be larger than 13yr cicadas on average. Koyama et al. [1] investigate geographic body size clines for 7 species of periodical cicadas in eastern North America, whose phylogenetic relationships are resolved, in a life history context, using an impressively large number of populations (Fig. 1 of [1]). The authors report generally female-biased sexual body size dimorphism (SSD), and (however not for all species) a positive relationship of body size with habitat annual mean temperature taken from weather data and a negative correlation with latitude (Fig. 3 of [1]). The latter is consistent with a converse Bergmann cline. Crucially, body size of two at least partly sympatric 13y & 17y sister species pairs did not differ (by much), contrary to expectation because the 17y species have more time to grow larger. 13y cicadas must therefore generally grow faster (or 17y cicadas slower) to in the end acquire the same (optimal?) body size. The phylogenetically oldest 13y cicada species, however, is larger, suggesting that selection for large (optimal?) body size has relaxed over evolutionary time, for unknown reasons (about which the authors speculate). A mechanistic explanation for this phenomenon is suggested based on the hypothesis that 17y cicadas simply arrest or slow down growth early during their juvenile stage to delay emergence for 4 further years (Fig. 2 of [1]).
We think this is an impressive data set, and the life history question addressed in this prominent insect taxon should appeal to readers generally interested in whole-organism evolution despite being largely descriptive.

Reference

[1] Koyama T, Ito H, Kakishima S, Yoshimura J, Cooley JR, Simon C, Sota T. 2015. Geographic body size variation in the periodical cicadas Magicicada: implications for life cycle divergence and local adaptation. Journal of Evolutionary Biology 28:1270-1277. doi: 10.1111/jeb.12653

It is well known that the rearing environment has strong effects on life history and fitness traits of organisms. Microbes are part of every environment and as such likely contribute to such environmental effects. Gut bacteria are a special type of microbe that most animals harbor, and as such they are part of most animals’ environment. Such microbial symbionts therefore likely contribute to local adaptation [1]. The main question underlying the laboratory study by Guilhot et al. [2] was: How much do particular gut bacteria affect the organismal phenotype, in terms of life history and larval foraging traits, of the fruit fly Drosophila melanogaster, a common laboratory model species in biology?
To investigate the above question, the authors isolated 4 taxa of bacteria from the gut of a (randomly picked) Drosophila melanogaster lab strain, and subsequently let Drosophila melanogaster eggs and larvae (stemming from their own, different lab strain) develop both in the typical artificial laboratory medium as well as in grapes, a natural “new” habitat for Drosophila larvae, inoculated with theses bacteria, singly and in combination, also including a bacteria-free control. By investigating various relevant developmental and size traits, the authors found that adding particularly Enterobacteria had some visible effects on several traits, both upward (indicting improvement) and downward (being detrimental) (with three other types of bacteria showing only minor or even no effects). In general, the grape medium reduced performance relative to the standard lab medium. Strongest interactive effects occurred for development time and body size, together making up growth plasticity [3], with lesser such effects on some related behavioral (feeding) traits (Figs. 2,3).
The study premise is interesting, its general objectives are clearly laid out, and the practical work was conducted correctly as far as I can evaluate. The study remains largely descriptive in that no particular a priori hypotheses or predictions in relation to the specific bacteria isolated were formulated, not least because the bacteria were necessarily somewhat arbitrarily chosen and there were apparently no prior studies from which to derive concrete predictions. Overall, the results of this study should be of interest to the community of evolutionary ecologists, especially those working on nutritional and microbiome effects on animal life histories. I consider this work to be primarily ecological, with limited evolutionary content (e.g. no genetics) though some evolutionary implications, as mentioned in the paper’s Conclusions. So this paper would best fit in a microbial or physiological ecology outlet/journal.
The inclusion of a natural medium (grapes) must be commended because this permits inferences and conclusions for at least one natural environment, whereas inferences drawn from laboratory studies in the artificial medium that most Drosophila researchers seem to use are typically limited. Unsurprisingly perhaps, the study showed that Drosophila melanogaster fared generally better in the artificial than the chosen natural medium (grape). Crucially, however, the bacterial symbionts modified both media differentially. Although common bacterial taxa were chosen, the particular bacteria isolated and used remain arbitrary, as there are many. I note that the main and strongest interactive effects between medium and bacterial type are apparent for the Enterobacteria, and they probably also strongly, if not exclusively, mediate the overall effect of the bacterial mixture.
While these specific data are novel, they are not very surprising. If we grow animals in different environments we can expect some detectable effects of these environments, including the bacterial (microbiome) environment, on the hosts life history. The standard and predicted [4] life history response of Drosophila melanogaster (but not all insects [3]) facing stressful nutritional environments, as apparently created by the Enterobacteria, is to extend development but come out smaller in the end. This is what happened here for the laboratory medium ([2]: Fig. 5). The biological interpretation is that individuals have more trouble ingesting and/or digesting the nutrients available (thus prolonging their foraging period and development), yet cannot convert the nutrients effectively into body size increments (hence emerging smaller). This is what the authors here refer to as developmental plasticity, which is ultimately nutritionally mediated. However, interestingly, a signal in the opposite direction was indicated for the bacterial mixture in the grape medium (flies emerging larger after accelerated development: Fig. 5), suggesting some positive effects on growth rate of the natural medium, perhaps related to grapes being a limited resource that needs to be escaped quickly [3]? The reversal of sexual size dimorphism across bacterial treatments in the grape environment detectable in Fig. 4 is interesting, too, though I don’t understand why this happens, and this is not discussed.
In general, more encompassing and increased questions in this context to be researched in the future could be: 1) are these effects predictable (not (yet) at this point, or so it seems); and 2) how strong are these environmental bacterial effects relative to other, more standard effects (e.g. relative to genetic variation, population variation, etc., or relative to other types of environmental effects like, say, temperature)? (3) It could further be asked why not natural but laboratory populations of Drosophila were used for this experiment, if the aim was to draw inferences for the wild situation. (4) Although Genotype x Environment effects are invoked in the Discussion, they were not tested here, lacking genetically different Drosophila families or populations. From an evolutionary standpoint, I consider this the greatest weakness of the study. I was also not too thrilled by the particular statistical analyses employed, though this ultimately does not negate the results. Nevertheless, this work is a good start in this huge field investigating the microbiome. In conclusion, I can recommend this paper after review by PCI Evol Biol.

References

[1] Kawecki, T. J. and Ebert, D. (2004) Conceptual issues in local adaptation. Ecology Letters 7: 1225-1241. doi: 10.1111/j.1461-0248.2004.00684.x
[2] Guilhot, R., Rombaut, A., Xuéreb, A., Howell, K. and Fellous, S. (2019). Environmental specificity in Drosophila-bacteria symbiosis affects host developmental plasticity. BioRxiv, 717702, v3 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/717702
[3] Blanckenhorn, W.U. (1999) Different growth responses to temperature and resource limitation in three fly species with similar life histories. Evolutionary Ecology 13: 395-409. doi: 10.1023/A:1006741222586
[4] Stearns, S. C. and Koella, J. (1986) The evolution of phenotypic plasticity in life history traits: predictions of reaction norms for age and size at maturity. Evolution 40: 893-914. doi: 10.1111/j.1558-5646.1986.tb00560.x