Decoupled maternal and zygotic genetic effects shape the evolution of development

Evolutionary transitions from indirect to direct development involve changes in both maternal and zygotic genetic factors, with distinctive population-genetic implications, but empirical data on the genetics of such transitions are lacking. The polychaete Streblospio benedicti provides an opportunity to dissect a major transition in developmental mode using forward genetics. Females in this species produce either small eggs that develop into planktonic larvae or large eggs that develop into benthic juveniles. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. The likely fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.

Evolutionary Development of Marine Larvae

Access to a growing number of marine invertebrates with genetic and genomic tools has broadened our understanding of the diversity of developmental mechanisms, informing our understanding of larval evolution by allowing the identification of shared or divergent programs for the formation of body plan patterning and organ formation. Two such genetic programs are the apical plate patterning network and the hox/parahox trunk and gut patterning network common to larval and adult forms, respectively. While mounting evidence supports an ancient origin at the base of the Bilateria for both adult and larval forms, it is clear that many distinct organs and structures have appeared independently and can be shifted between the larval and adult phase frequently. Future advances in our understanding of larval evolution are likely to emerge from exhaustive studies of marine invertebrate cell types by single-cell sequencing technologies and through the study of the genetic basis of the metamorphic transition.

A possible 150 million years old cirripede crustacean nauplius and the phenomenon of giant larvae

The larval phase of metazoans can be interpreted as a discrete post-embryonic period. Larvae have been usually considered to be small, yet some metazoans possess unusually large larvae, or giant larvae. Here, we report a possible case of such a giant larva from the Upper Jurassic Solnhofen Lithographic limestones (150 million years old, southern Germany), most likely representing an immature cirripede crustacean (barnacles and their relatives). The single specimen was documented with up-to-date imaging methods (macro-photography, stereo-photography, fluorescence photography, composite imaging) and compared with modern cirripede larvae. The identification is based on two conspicuous spine-like extensions in the anterior region of the specimen strongly resembling the so-called fronto-lateral horns, structures exclusively known from cirripede nauplius larvae. Notably, at 5 mm in length the specimen is unusually large for a cirripede nauplius. We therefore consider it to be a giant larva and discuss possible ecological and physiological mechanisms leading to the appearance of giant larvae in other lineages. Further findings of fossil larvae and especially nauplii might give new insights into larval evolution and plankton composition in the past.

Decoupled Maternal and Zygotic Genetic Effects Shape the Evolution of Development

Many animals develop indirectly via a larval stage that is morphologically and ecologically distinct from its adult form. Hundreds of lineages across animal phylogeny have secondarily lost larval forms, instead producing offspring that directly develop into adult form without a distinct larval ecological niche1–7. Indirect development in the sea is typically planktotrophic: females produce large numbers of small offspring that require exogenous planktonic food to develop before metamorphosing into benthic juveniles. Direct development is typically lecithotrophic: females produce a smaller number of larger eggs, each developing into a juvenile without the need for larval feeding, provisioned by yolk. Evolutionary theory suggests that these alternative developmental strategies represent stable alternative fitness peaks, while intermediate states are disfavored4,8–11. Transitions from planktotrophy to lecithotrophy thus require crossing a fitness valley and represent radical and coordinated transformations of life-history, fecundity, ecology, dispersal, and development7,12–16. Here we dissect this transition in Streblospio benedicti, the sole genetically tractable species that harbors both states as heritable variation17–19. We identify large-effect loci that act maternally to influence larval size and independent, unlinked large-effect loci that act zygotically to affect discrete aspects of larval morphology. Because lecithotrophs and planktotrophs differ in both size and morphology, the genetic basis of larval form exhibits strong maternal-by-zygotic epistasis for fitness20. The fitness of zygotic alleles depends on their maternal background, creating a positive frequency-dependence that may homogenize local populations. Developmental and population genetics interact to shape larval evolution.