Decoupled maternal and zygotic genetic effects shape the evolution of development.

Christina Zakas,Alex D Kay,Jennifer M Deutscher,Matthew V Rockman

doi:10.7554/elife.37143

Abstract

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.

Highlights

Many animals develop indirectly via larval stages that are morphologically and ecologically distinct from their adult forms
We find that co-adapted life-history traits are strikingly modular, where each of the phenotypes has a largely independent genetic basis with QTL occurring on different chromosomes
Maternally-determined larval size has an independent genetic basis from other traits that are perfectly correlated in natural populations

Summary

Introduction

Many animals develop indirectly via larval stages that are morphologically and ecologically distinct from their adult forms. Transitions from planktotrophy to lecithotrophy represent radical and coordinated transformations of life-history, fecundity, ecology, dispersal, and development (Duda and Palumbi, 1999; Jeffery and Emlet, 2003; McEdward and Miner, 2001; Raff, 1996; Romiguier et al, 2014; Wray, 1995). We dissect this transition in the polychaete annelid Streblospio benedicti, a genetically tractable species that harbors both states as heritable variation (Levin, 1984; Levin et al, 1991; Zakas and Rockman, 2014)

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Conclusion