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Laboratory evolution of flies to morphogen dosage via rapid maternal changes reveals predictable outcomes

Xueying C. Li, Lautaro Gandara, Måns Ekelöf, Kerstin Richter, Theodore Alexandrov, Justin Crocker

Preprint posted on 30 September 2022 https://www.biorxiv.org/content/10.1101/2022.09.28.509860v2

To ‘big embryo’ (BE), or not to BE, that’s the question

Selected by Girish Kale

Background:

When a mother produces an egg, it is packed with nutrients that will be required for the development of the embryo. Naturally, we can expect that there will be some sort of calculation that will decide how many eggs a mother can produce at a time, depending on how much nutrients are required per embryo and the total availability of nutrients for the purposes of reproduction. The egg also contains the necessary information to allow the embryo to figure out its body axes. With this information, the embryo is able to fairly distribute its resources towards formation of different structures and organs. Thus, as far as utilization of resources is concerned, both the mother and the embryo are constrained: the mother needs to strike a balance between producing a few large embryos vs. many small embryos, while the embryo needs to reasonably allocate its resources across all the organs it will generate.

If there is a change in the allocation of resources towards the formation of different organs in the embryo, then that can produce a massive burden on embryonic development and eventually result in its failure. What happens if the embryo is forced to redistribute its resources? We can expect that its development will be defective, which leads to reduced embryo survival. But, as we all know, “Life breaks free…. Painfully, perhaps even dangerously. But life finds a way.” So, how will the conundrum of nutrient allocation be solved? Let’s find out!

Key findings:

In this preprint, the authors used the genetic model organism Drosophila melanogaster, the fruit fly. There is extensive literature on embryonic patterning in Drosophila embryos, which allowed the authors to identify and use the simplest possible manipulations to change the proportions of the resources that are allocated to the head vs. the trunk of the embryo. The authors demonstrated that having 2 extra copies of the gene bicoid (4 copies in total) shifts the head-trunk boundary to produce a larger head domain, at the expense of trunk domain, while the embryo itself remains the same size. A lack of change in overall embryo size is not surprising, as this is dictated by the mother. The authors further showed that having such a redistribution of embryo domains also leads to reduction in embryo survival.

So, the stage is set: we have the conundrum that life needs to solve. At this point, the authors went for an EMS mutagenesis approach: creating a lot of random mutations, some of which could, in theory, improve embryo survival with a classical “survival of the fittest” selection. Think of this approach as shooting enough arrows in the dark such that some will hit the target. Starting from such a mutated population of flies, the authors let the selection experiment run, while keeping an eye on various parameters that would indicate an increase in embryo survival, as well as changes in the size of the head. Excitingly, the authors found that there is a shift in the location of the head-trunk boundary. Surprisingly, the shift in the boundary is due to an increase in embryo size! In other words, the mutations that end up increasing embryo fitness involve changes in the way the mothers produce the embryos.

The authors then performed a nuanced analysis of the various changes that occurred over the course of the selection experiment, or using the earlier analogy, all the arrows that had hit their target. A key change that they observed consistently related to metabolic regulation. The balance had now been shifted! The mothers now produced a few large embryos rather than many small embryos. Here, the authors asked if their observations resembled what could be happening in nature. Again, knowledge of natural populations of Drosophila melanogaster came in handy: the authors compared two isolates of natural populations, one having larger embryos than the other. As their results would predict, the population with larger embryos has more bicoid, and their mothers produce fewer embryos.

Emboldened by their success so far, the authors decided to push even further, and asked whether the balance between the size and number of embryos is a universal phenomenon. Instead of limiting themselves to various natural populations of the same species, now the authors compared multiple species within the Drosophila family. They could see a nice (negative) correlation between the size and number of eggs. In other words, species that produce larger eggs, also produce fewer eggs, while species producing smaller eggs will produce more eggs.

Importance of the findings:

This preprint once again demonstrates the strength of the fruit fly model organism, as an experimental playground to address rather complicated questions about metabolic regulation. The study also shows how rapidly an organism can evolve, not only to accommodate for genetic mutations, but also to the environment. One can expect similar levels of plasticity to change the balance between size and number of eggs, if the total nutrients were to change as well. The study further highlights the potential for laboratory selection to mimic natural selection. Such experiments, for instance, could be useful to understand what would be the fate of various species in a changing environment, especially relevant in the context of global warming.

Questions to authors:

1) As we can imagine, the availability of nutrients will depend on the season. How do you think such variability will affect the size vs. the number of eggs? Would you expect that only one of these will be affected or both?

2) You have extended your observations in Drosophila melanogaster to other Drosophila species in the family of fruit flies, to see whether they also have a similar balance between ovariole size and number. Do you think this can be extended beyond the fruit flies? If so, would you expect to see a common trend across various fly species, or would there be different trends between various families of species? In this context, how do you interpret the correlation between ecology and egg size across all insects, as reported in Church et al. 2019?

Tags: drosophila melanogaster, early embryonic development, laboratory evolution, metabolic regulation, oogenesis, pattern formation

Posted on: 2 April 2023

doi: https://doi.org/10.1242/prelights.34203

Read preprint (No Ratings Yet)

Author's response

Xueying C. Li shared

1) Yes, it is highly possible that reproductive traits such as the size and the number of eggs vary with seasons. Actually, a study last year by Rudman et al. has elegantly demonstrated it in a common-garden experiment, revealing seasonal changes in many traits including egg size. We would be curious to see if the relationship between size and number varies with season as well.

2) Actually, we found that the correlation between the size and the number of eggs decayed when we extended the analysis to more distantly related Drosophila species, which might be indeed explained by the differences in ecology between them. Therefore, we think one might be able to find such relationships within groups of closely related species, but different groups of species might show different trends. It would be very interesting to investigate this relationship while grouping the species based on their ecological context.

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