Implications of shifting egg size in different phyla

I completed a postdoc in Marty Kreitman’s lab in the Department of Ecology and Evolution at The University of Chicago in 2011.  There I used several techniques to visualize the way that different selective pressures on egg size affect the spatial patterning of developing Drosophila embryos.  One cycle 14 embryo double stained for mRNA of the gap gene giant and the nuclear stain Sytox green is shown above in the upper panel.  I used artificial selection to generate large and small egg lines and triple stained these embryos for giant (gt), and even-skipped (eve), and with Sytox green as a nuclear stain.  I used some innovative software called PointCloudToolbox to compare the eve stripe patterns between the divergently selected lines, as well as number of nuclei at the periphery for mitotic cycle 14 embryos.  I got some interesting results (Miles et al. 2011).  Border positions of some of the 7 stripes of eve were shifted in the large-egg lines relative to controls and small-egg embryos. Some of our collaborators at Cincinnati Children’s Hospital (David Cheung in Jun Ma’s Lab) used these same flies, as well as some inbred lines derived from these populations, to examine differential allocation of the morphogen Bicoid in eggs of different sizes.  Our collaboration led to a pair of papers in Development (Cheung et al. 2011; 2014). I generated multiple inbred sublines from my selected populations and have now looked at the expression of some of the terminal gap genes in these flies to explore the mechanism behind my earlier results. I hope to extend this work with my collaborator Manu, at the University of North Dakota. Another fascinating aspect of this artificial selection experiment was recently published in MBE, together with our collaborator Aashish Jha (Jha et al. 2015). Using whole-genome resequencing, we were able to identify 110 candidate genes underlying the highly polygenic trait of egg size. Some surprises in that list, too!

My interest in egg size, or per offspring maternal provisioning, began with two identical populations of sea slugs found in the Florida Keys and the Caribbean.  The adults look identical but their ecological niches and their life histories are not.  One population produces many small eggs and develops indirectly, with a feeding larval stage.  One of their spiral egg masses is pictured above.  The other produces fewer, larger eggs and hatches as a juvenile directly from the egg mass.  I used histochemistry, biochemistry, and calorimetry to compare these egg masses while working on my Master’s degree at Florida Institute of Technology.   I concluded that the major difference between the two was deposition of extra-embryonic glycoprotein in the capsular fluid of the direct developer, allowing flexibility of developmental mode between the two populations (Miles and Clark 2002). Patrick Krug, at Cal State LA, has been following up on whether this is a truly poecilogonous species, developmental plasticity, or cryptic speciation. 

Next, I collaborated with labmates to extend the question of effects of egg size to include other aspects of life history, juvenile quality and total development time, by manipulating food levels encountered during larval development in obligate planktotrophic echinoids with different egg sizes.  We found a two-fold benefit of feeding during specified periods of larval development for the small-egg species under high food conditions only, which developed more quickly and produced higher quality juveniles (Reitzel et al. 2005).   

As part of my dissertation work with Marta Wayne at the University of Florida, I examined the genetic basis for egg size evolution, by using various quantitative genetic techniques to estimate narrow-sense heritability for egg size in a polychaete worm (Miles et al. 2007).  The spherical golden brown eggs are pictured above.  I also performed artificial selection on egg size and measured multiple fitness-related traits across the life history in this hermaphroditic marine worm.   Surprisingly, large-egg mothers were more fecund and produced larger competent larvae, while also changing sex from male to female earlier than control line individuals.  We hypothesized  a trade-off between male and female fitness with respect to egg size (Miles and Wayne 2008).  

I think you can see that the trait of egg size intersects with many different fields of inquiry.  This is a trait that is very closely tied to the fitness of both offspring and adults.  “Decisions” about what, how much, and how often to allocate resources to offspring have important implications that intertwine with life history evolution, phenotypic plasticity, developmental robustness, speciation, and interactions between genetic and environmental variability.  Egg size is a classic quantitative trait that has a great deal to teach us about diverse topics and how they intersect at the phenotypic level.