These worms develop differently depending on their parents’ genes — even the ones they don’t inherit

(A) A small, plankton-hunting larva, also known as a planktotroph; (B) A large larva or lecithotroph, that has no appendages; (C) and (D) are two examples of larvae with intermediate phenotypes between (A) and (B). Photographs taken at 20X magnification by Conor Gilligan, a graduate student in the Rockman lab.

The following is a guest post by Ornob Alam, a graduate student in Michael Purugganan’s lab at New York University. Ornob’s PhD projects examine the demographic and evolutionary history of domesticated Asian rice in the context of past climate change and human migrations; he is on Twitter as @genomeinquirer.

Female ocean sunfish release up to 300 million eggs into the water during spawning to be met by similarly large numbers of sperm released by the males. This marks the end of their parental investment, leaving newly fertilized offspring to fend for themselves and mostly die. The ocean sunfish reproductive strategy stands in stark contrast to our own, where the offspring first develops inside the mother and parents pour extensive resources into raising a small number of offspring to adulthood.

How did animals come to have such divergent life histories? This question is deeply entwined with inquiries into the evolution of novel modes of post-fertilization development, and at the heart of a recent study in Evolution that explored the genetic bases of different modes of development occurring in a single species of marine worms.

Matt Rockman, a co-author of the study, first began studying these worms – called Streblospio benedicti – in his lab at New York University in 2008. It is one of many species of worms he studies to address various evolutionary questions. 

Streblospio benedicti is particularly well-suited for the study of radical changes in development, says Rockman. Different populations of the worm typically undergo either of two very distinct developmental modes: an indirect mode characterized by the production of large number of very small larvae that have appendages to defend from predation and must hunt for food, and a direct mode involving greater investment into a small number of large larvae that do not need to hunt, and develop directly into their adult morphology.

Identifying the genetic bases of developmental modes is key to uncovering how they evolved. Species like S. benedicti that have multiple developmental modes allow observation of possible intermediate states and can help reveal what genetic changes are required for evolutionary transitions between modes. 

Rockman started work on the current study with co-author Christina Zakas, now an assistant professor at North Carolina State University, when she was a postdoc in his lab. They performed three rounds of crosses, the first between two worms from isolated populations that each exclusively go through one of the two developmental modes. They genotyped all individuals until the third generation – the offspring from the second round of crosses – using a targeted sequencing approach and looked for associations between larval traits and genomic loci in not just the larvae themselves but also in the parents.  

In a first batch of results from the crossing experiment, the authors had already reported that larval size was determined by variants in specific loci in the mothers’ genomes while larval appendage traits – including their number and length – depended on a small number of offspring loci. For the Evolution study, they newly recorded and incorporated larval appendage traits for almost 4000 offspring from the fourth generation of the pedigree.

The authors were able to reproduce the findings on maternal and offspring genetic effects from the previous study. In addition, they tested for and found paternal effects: two alleles, if present in the mother, were likely to produce larger larvae — but their presence in the father was associated with smaller progeny. It appears that larval traits, which are associated with the type of developmental mode, depend on loci in all three of the mother, father, and offspring in these worms.

The findings from this study may go some way toward explaining why individual populations of S. benedicti usually exhibit one of the two developmental modes. Intermediate larval forms have rarely been observed in the wild, even though they readily arise from crosses like the one in this study, implying some major fitness cost to intermediacy in the worms’ ecological contexts. If larval traits and fitness are partially dependent on parental genomes, a mismatch between offspring and parental genomes would lead to intermediates with low fitness. The developmental mode that is at a higher frequency in a population is thus likely to increase further in frequency as mating between individuals of the same type would produce more fit offspring. 

Once a developmental mode becomes fixed in a population, it would be expected to remain that way even with some influx of divergent individuals. Underlying this expectation, of course, is the assumption that intermediate larvae get selected against. This has not been directly demonstrated, which is something Rockman intends to change.

Conor Gilligan, a graduate student in his lab, has begun to investigate rare populations in which individuals with both direct and indirect developmental modes coexist, says Rockman. “We can basically look for genotype frequency differences between adults that are settled and their larvae,” he notes, which would allow them to ask whether individuals of different developmental types are indeed mating, and whether certain larval genotypes or phenotypes never make it into adulthood.

In accounting for parental effects in their recent work, the authors have expanded the question of what genomic regions determine developmental mode to also include whose genomic regions. Parental genomic loci influencing offspring traits is not unique to these worms and likely occurs in many, if not most, organisms. For instance, parental effects have long been known to be present in humans, and another recent study teased apart the contributions of human parental and fetal genomes to fetal growth and eventual birth weight.

While the current findings do not directly address the origin of novel developmental modes, they point to mechanisms that can maintain developmental variation in a single species and result in loss of the same variation in individual populations of the species. Future work looking at wild populations of the worm will be key to understanding the ecological forces that select for different developmental modes and may have contributed to their emergence.

About Jeremy Yoder

Jeremy B. Yoder is an Associate Professor of Biology at California State University Northridge, studying the evolution and coevolution of interacting species, especially mutualists. He is a collaborator with the Joshua Tree Genome Project and the Queer in STEM study of LGBTQ experiences in scientific careers. He has written for the website of Scientific American, the LA Review of Books, the Chronicle of Higher Education, The Awl, and Slate.
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