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

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

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

References

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

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

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

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

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

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

How do phenotypic plasticity and adaptive evolution interact in a novel or changing environment? Does evolution by natural selection generally reinforce initially plastic phenotypic responses, or does it instead oppose them? And to what extent does evolution of a trait involve evolution of its plasticity? These questions have lied at the heart of research on phenotypic evolution in heterogeneous environments ever since it was realized that the environment is likely to affect the expression of many (perhaps most) characters of an individual. Importantly, this broad definition of phenotypic plasticity as change in the average phenotype of a given genotype in response to its environment of development (or expression) does not involve any statement about the adaptiveness of the plastic changes. Theory on the evolution of plasticity has devoted much effort to understanding how reaction norm should evolve under different regimes of environmental change in space and time, and depending on genetic constraints on reaction norm shapes. However on an empirically ground, the questions above have mostly been addressed for individual traits, often chosen a priori for their likeliness to exhibit adaptive plasticity, and we still lack more systematic answers. These can be provided by so-called ‘phenomic’ approaches, where a large number of traits are tracked without prior information on their biological or ecological function. A problem is that the number of phenotypic characters that can be measured in an organism is virtually infinite (and to some extent arbitrary), and that scaling issues makes it difficult to compare different sets of traits. Gene-expression levels offer a partial solution to this dilemma, as they can be considered as a very large number of traits (one per typed gene) that can be measured easily and uniformly (fold change in the number of reads in RNAseq). As for any traits, expression levels of different genes may be genetically correlated, to an extent that depends on their regulation mechanism: cis-regulatory sequences that only affect expression of neighboring genes are likely to cause independent gene expression, while more systematic modifiers of expression (e.g. trans-regulators such as transcription factors) may cause correlated genetic responses of the expression of many genes. Huang and Agrawal [1] have studied plasticity and evolution of gene expression level in young larvae of populations of Drosophila melanogaster that have evolved for about 130 generations under either a constant environment (salt or cadmium), or an environment that is heterogeneous in time or space (combining salt and cadmium). They report a wealth of results, of which we summarize the most striking here. First, among genes that (i) were initially highly plastic and (ii) evolved significant divergence in expression levels between constant environment treatments, the evolved divergence is predominantly in the opposite direction to the initial plastic response. This suggests that either plasticity was initially maladaptive, or the selective pressure changed during the evolutionary process (see below). This somewhat unexpected result strikingly mirrors that from a study published last year in Nature [2], where the same pattern was found for responses of guppies to the presence of predators. However, Huang and Agrawal [1] went beyond this study by deciphering the underlying mechanisms in several interesting ways. First, they showed that change in gene expression often occurred at genes close to SNPs with differentiated frequencies across treatments (but not at genes with differentiated SNPs in their coding sequences), suggesting that cis-regulatory sequences are involved. This is also suggested by the fact that changes in gene expression are mostly caused by the increased expression of only one allele at polymorphic loci, and is a first step towards investigating the genetic underpinnings of (co)variation in gene expression levels. Another interesting set of findings concerns evolution of plasticity in treatments with variable environments. To compare the gene-expression plasticity that evolved in these treatments to an expectation, the authors considered that the expression levels in populations maintained for a long time under constant salt or cadmium had reached an optimum. The differences between these expression levels were thus assumed to predict the level of plasticity that should evolve in a heterogeneous environment (with both cadmium and salt) under perfect environmental predictability. The authors showed that plasticity did evolve more in the expected direction in heterogeneous than in constant environments, resulting in better adapted final expression levels across environments. Taken collectively, these results provide an unprecedented set of patterns that are greatly informative on how plasticity and evolution interact in constant versus changing environments. But of course, interpretations in terms of adaptive versus maladaptive plasticity are more challenging, as the authors themselves admit. Even though environmentally determined gene expression is the basic mechanism underlying the phenotypic plasticity of most traits, it is extremely difficult to relate to more integrated phenotypes for which we can understand the selection pressures, especially in multicellular organisms. The authors have recently investigated evolutionary change of quantitative traits in these selected lines, so it might be possible to establish links between reaction norms for macroscopic traits to those for gene expression levels. Such an approach would also involve tracking gene expression throughout life, rather than only in young larvae as done here, thus putting phenotypic complexity back in the picture also for expression levels. Another difficulty is that a plastic response that was originally adaptive may be replaced by an opposite evolutionary response in the long run, without having to invoke initially maladaptive plasticity. For instance, the authors mention the possibility that a generic stress response is initially triggered by cadmium, but is eventually unnecessary and costly after evolution of genetic mechanisms for cadmium detoxification (a case of so-called genetic accommodation). In any case, this study by Huang and Agrawal [1], together with the one by Ghalambor et al. last year [2], reports novel and unexpected results, which are likely to stimulate researchers interested in plasticity and evolution in heterogeneous environments for the years to come.

References

[1] Huang Y, Agrawal AF. 2016. Experimental Evolution of Gene Expression and Plasticity in Alternative Selective Regimes. PLoS Genetics 12:e1006336. doi: 10.1371/journal.pgen.1006336

[2] Ghalambor CK, Hoke KL, Ruell EW, Fischer EK, Reznick DN, Hughes KA. 2015. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525: 372-375. doi: 10.1038/nature15256

Spatial population genetics is a field that studies how different evolutionary processes shape geographical patterns of genetic variation. This field is currently hampered by the lack of a deep understanding of the impact of different evolutionary processes shaping the genetic diversity observed across a continuous space (Bradburd and Ralph 2019). Luckily, the recent development of slendr (Petr et al. 2023), which uses the simulator SLiM (Haller and Messer 2023), provides a powerful tool to perform simulations to analyze the impact of different evolutionary parameters on spatial patterns of genetic variation. Here, Ianni-Ravn, Petr, and Racimo 2023 present a series of well-designed simulations to study how three evolutionary factors (dispersal distance, competition distance, and mate choice distance) shape the geographical structure of genealogies.

The authors model the dispersal distance between parents and their offspring using five different distributions. Then, the authors perform simulations and they contrast the correspondence between the distribution of observed parent-offspring distances (called DD in the paper) and the distribution used in the simulations (called DF). The authors observe a reasonable correspondence between DF and DD. The authors then show that the competition distance, which decreases the fitness of individuals due to competition for resources if the individuals are close to each other, has small effects on the differences between DD and DF. In contrast, the mate choice distance (which specifies how far away can a parent go to choose a mate) causes discrepancies between DD and DF. When the mate choice distance is small, the individuals tend to cluster close to each other. Overall, these results show that the observed distances between parents and offspring are dependent on the three parameters inspected (dispersal distance, competition distance, and mate choice distance) and make the case that further ecological knowledge of each of these parameters is important to determine the processes driving the dispersal of individuals across geographical space. Based on these results, the authors argue that an “effective dispersal distance” parameter, which takes into account the impact of mate choice distance and dispersal distance, is more prone to be inferred from genetic data.

The authors also assess our ability to estimate the dispersal distance using genealogical data in a scenario where the mating distance has small effects on the dispersal distance. Interestingly, the authors show that accurate estimates of the dispersal distance can be obtained when using information from all the parents and offspring going from the present back to the coalescence of all the individuals to the most recent common ancestor. On the other hand, the estimates of the dispersal distance are underestimated when less information from the parent-offspring relationships is used to estimate the dispersal distance.

This paper shows the importance of considering mating patterns and the competition for resources when analyzing the dispersal of individuals. The analysis performed by the authors backs up this claim with carefully designed simulations. I recommend this preprint because it makes a strong case for the consideration of ecological factors when analyzing the structure of genealogies and the dispersal of individuals. Hopefully more studies in the future will continue to use simulations and to develop analytical theory to understand the importance of various ecological processes driving spatial genetic variation changes.

References

Bradburd, Gideon S., and Peter L. Ralph. 2019. “Spatial Population Genetics: It’s About Time.” Annual Review of Ecology, Evolution, and Systematics 50 (1): 427–49. https://doi.org/10.1146/annurev-ecolsys-110316-022659.

Haller, Benjamin C., and Philipp W. Messer. 2023. “SLiM 4: Multispecies Eco-Evolutionary Modeling.” The American Naturalist 201 (5): E127–39. https://doi.org/10.1086/723601.

Ianni-Ravn, Mariadaria K., Martin Petr, and Fernando Racimo. 2023. “Exploring the Effects of Ecological Parameters on the Spatial Structure of Genealogies.” bioRxiv, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.03.27.534388.

Petr, Martin, Benjamin C. Haller, Peter L. Ralph, and Fernando Racimo. 2023. “Slendr: A Framework for Spatio-Temporal Population Genomic Simulations on Geographic Landscapes.” Peer Community Journal 3 (e121). https://doi.org/10.24072/pcjournal.354.

Despite a vast array of ways in which organisms can reproduce (Bell, 1982), most animals engage in sexual reproduction (Otto & Lenormand, 2002). A fascinating alternative to sex is parthenogenesis, where offspring are produced asexually from a gamete, typically the egg, without receiving genetic material from another gamete (Simon, Delmotte, Rispe, & Crease, 2003). One of the long-standing questions in the field is why parthenogenesis is not more widespread, given the costs associated with sex (Otto & Lenormand, 2002).  Natural populations of most species appear to be reproducing either sexually or parthenogenetically, even if a species can employ both reproductive modes (Larose et al 2023). Larose et al (2023) highlight the conundrum in this pattern, as organisms that are capable of employing parthenogenesis facultatively would be able to gain the benefits of both modes of reproduction. Why then, is facultative parthenogenesis not more common?

Larose et al (2023) propose that constraints on being efficient in both sexual and asexual reproduction could cause a trade-off between reproductive modes that favours an obligate strategy of either sex or no sex. This would provide an explanation for why facultative parthenogenesis is rare. Timema stick insects provide an excellent system to investigate reproductive strategies, as some species have parthenogenetic females, while other species are sexual, and they show repeated transitions from sexual reproduction to obligate parthenogenesis (Schwander & Crespi, 2009). The authors performed comprehensive and complementary studies in a recently discovered species T. douglasi, in which populations show both modes of reproduction, with some populations consisting only of females and others showing equal proportions of males and females. The sex ratio varied significantly, with the proportion of females ranging between 43-100% across 29 populations. These populations form a monophyletic clade with clustering into three genetic lineages and only a few cases of admixture. Females from all populations were capable of producing unfertilized eggs, but the hatching success varied hugely among populations and lineages (3-100%). Parthenogenetically produced offspring were homozygous, showing that parthenogenesis causes a complete loss of heterozygosity in a single generation. After producing eggs as virgins, females were mated to assess the capacity to also reproduce sexually, and fertilization increased the hatching success of eggs in two lineages. In one lineage, in which the hatching success of unfertilized eggs is similar to that of other sexually reproducing Timema species, fertilization reduced egg-hatching success, indicating a trade-off between reproductive modes with parthenogenetic reproduction performing best. Approximately 58% of the offspring produced after mating were fertilized, demonstrating the capacity of females to reproduce parthenogenetically also after mating has occurred, however with huge variation among individuals.

This wonderful and meticulously performed study produces strong and complementary evidence for facultative parthenogenesis in T. douglasi populations. The study shows large variation in how reproductive mode is employed, supporting the existence of a trade-off between sexual and parthenogenetic reproduction. This might be an example of an ongoing transition from sexual to asexual reproduction, which indicates that obligate parthenogenesis may derive via transient facultative parthenogenesis. 

REFERENCES

Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press. 635 p.

Otto, S. P., & Lenormand, T. (2002). Resolving the paradox of sex and recombination. Nature Reviews Genetics, 3(4), 252-261. https://doi.org/10.1038/nrg761

Schwander, T., & Crespi, B. J. (2009). Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution, 63(1), 84-103. 
https://doi.org/10.1111/j.1558-5646.2008.00524.x

Simon, J.-C., Delmotte, F., Rispe, C., & Crease, T. (2003). Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society, 79(1), 151-163. https://doi.org/10.1046/j.1095-8312.2003.00175.x

Larose, C., Lavanchy,  G., Freitas, S., Parker, D.J., Schwander, T. (2023) Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects? bioRxiv, 2022.03.25.485836, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.03.25.485836

Parasites can manipulate their host’s behaviour to ensure their own transmission. These manipulated behaviours may be outside the range of ordinary host activities [1], or alter the crucial timing and/or location of a host’s regular activity. Vantaux et al show that the latter is true for the human malaria parasite, Plasmodium falciparum [2]. They demonstrate that three species of Anopheles mosquito were 24% more likely to choose human hosts, rather than other vertebrates, for their blood feed when they harboured transmissible stages (sporozoites) compared to when they were uninfected, or infected with non-transmissible malaria parasites [2]. Host choice is crucial for the malaria parasite Plasmodium falciparum to complete its life-cycle, as their host range is much narrower than the mosquito’s for feeding; P. falciparum can only develop in hominids, or closely related apes [3].
The study only shows this stage-dependent parasite manipulation retrospectively (by identifying host type and parasite stage in mosquitoes after their blood feed [2]). There was no difference in the preferences of infectious (with sporozoites) or un-infectious (infected without sporozoites, or uninfected) mosquitoes between human versus cow hosts in a choice test [2]. This suggests that the final decision about whether to feed occurs when the mosquito is in close range of the host.
This, coupled with previous findings, shows that vector manipulation is a fine-tuned business, that can act at multiple stages of the parasite life-cycle and on many behaviours [4]. Indeed, mosquitoes with non-transmissible Plasmodium stages (oocysts) are more reluctant to feed than sporozoite-infected mosquitoes [5] as vectors can be killed by their host whilst feeding, doing so before they are ready to transmit is risky for the malaria parasite. Thus, it seems that Plasmodium is, to some extent, master of its vector; commanding it not to feed when it cannot be transmitted, to feed when it is ready to be transmitted and to feed on the right type of host. What does this mean for our understanding of malaria transmission and epidemics?
Vantaux et al use a mathematical model, parameterised using data from this experiment, to highlight the consequences of this 24% increase in feeding on humans for P. falciparum transmission. They show that this increase raises the number of infectious bites humans receive from 4 (if sporozoite-infected mosquitoes had the same probability as uninfected mosquitoes) to 14 (an increase in 250%), for mosquitoes with a 15-day life-span, at ratios of 1:1 mosquitoes to humans. Longer mosquito life-spans and higher ratios of mosquitoes to humans further increases the number of infectious bites.
These results [2] have important implications for epidemiological forecasting and disease management. Public health strategies could focus on possible ways to trap sporozoite-infected mosquitoes, mimicking cues they use to locate their human hosts, or identify the behaviour of mosquitoes harbouring non-yet infectious Plasmodium, and trap them before they bite. Moreover, the results of the model show that failing to take into account the preference for humans of sporozoite-infected mosquitoes could underestimate the size of pending epidemics.
An important question previously raised is whether Plasmodium-induced alteration in host behaviour really is manipulation, or just a side-effect of being infected [4,5]. The fact that Vantaux et al show that these altered feeding behaviours increases the likelihood of transmission, in that a sporozoite-infected mosquito is more likely to feed on a human, strongly suggests that it is adaptive for the parasite [2]. Ultimately, to show that it is manipulation would require the identification of molecular factors released by Plasmodium that are responsible for physiological changes in the mosquito [6].

References

[1] Thomas, F., Schmidt-Rhaesa, A., Martin, G., Manu, C., Durand, P., & Renaud, F. (2002). Do hairworms (Nematomorpha) manipulate the water seeking behaviour of their terrestrial hosts? Journal of Evolutionary Biology, 15(3), 356–361. doi: 10.1046/j.1420-9101.2002.00410.x
[2] Vantaux, A., Yao, F., Hien, D. F., Guissou, E., Yameogo, B. K., Gouagna, L.-C., … Lefevre, T. (2018). Field evidence for manipulation of mosquito host selection by the human malaria parasite, Plasmodium falciparum. BioRxiv, 207183 ver 6. doi: 10.1101/207183
[3] Prugnolle, F., Durand, P., Ollomo, B., Duval, L., Ariey, F., Arnathau, C., … Renaud, F. (2011). A Fresh Look at the Origin of Plasmodium falciparum, the Most Malignant Malaria Agent. PLOS Pathogens, 7(2), e1001283. doi: 10.1371/journal.ppat.1001283
[4] Cator, L. J., Lynch, P. A., Read, A. F., & Thomas, M. B. (2012). Do malaria parasites manipulate mosquitoes? Trends in Parasitology, 28(11), 466–470. doi: 10.1016/j.pt.2012.08.004
[5] Cator, L. J., George, J., Blanford, S., Murdock, C. C., Baker, T. C., Read, A. F., & Thomas, M. B. (2013). “Manipulation” without the parasite: altered feeding behaviour of mosquitoes is not dependent on infection with malaria parasites. Proceedings. Biological Sciences, 280(1763), 20130711. doi: 10.1098/rspb.2013.0711
[6] Herbison, R., Lagrue, C., & Poulin, R. (2018). The missing link in parasite manipulation of host behaviour. Parasites & Vectors, 11. doi: 10.1186/s13071-018-2805-9