Does a complex life cycle affect adaptation to environmental change? Genome-informed insights for characterizing selection across complex life cycle.

Mary A. Sewell,Laetitia G. E. Wilkins,Katie E. Lotterhos,Adam M. Reitzel,Matthew P. Hare,Stacy A. Krueger-Hadfield,Holly K. Kindsvater,Samuel M. Bashevkin,Matthew W. Hahn,Molly A. Albecker

doi:10.1098/rspb.2021.2122

Abstract

Complex life cycles, in which discrete life stages of the same organism differ in form or function and often occupy different ecological niches, are common in nature. Because stages share the same genome, selective effects on one stage may have cascading consequences through the entire life cycle. Theoretical and empirical studies have not yet generated clear predictions about how life cycle complexity will influence patterns of adaptation in response to rapidly changing environments or tested theoretical predictions for fitness trade-offs (or lack thereof) across life stages. We discuss complex life cycle evolution and outline three hypotheses—ontogenetic decoupling, antagonistic ontogenetic pleiotropy and synergistic ontogenetic pleiotropy—for how selection may operate on organisms with complex life cycles. We suggest a within-generation experimental design that promises significant insight into composite selection across life cycle stages. As part of this design, we conducted simulations to determine the power needed to detect selection across a life cycle using a population genetic framework. This analysis demonstrated that recently published studies reporting within-generation selection were underpowered to detect small allele frequency changes (approx. 0.1). The power analysis indicates challenging but attainable sampling requirements for many systems, though plants and marine invertebrates with high fecundity are excellent systems for exploring how organisms with complex life cycles may adapt to climate change.

Highlights

Across eukaryotes, there is a myriad of different life cycle types that can include complex morphological changes within a single ploidy stage or among ploidy stages [1,2,3,4]
We discuss complex life cycle evolution and outline three hypotheses—ontogenetic decoupling, antagonistic ontogenetic pleiotropy and synergistic ontogenetic pleiotropy—for how selection may operate on organisms with complex life cycles
Because organisms with single ploidy stages can develop from the same genome, trade-offs among stages are expected to be common

Summary

Introduction

There is a myriad of different life cycle types that can include complex morphological changes within a single ploidy stage (e.g. metamorphosis) or among ploidy stages (e.g. haplodiplontic life cycles) [1,2,3,4]. The potential for life cycles to promote or constrain adaptation to changing environments remains a significant gap in predicting organisms’ vulnerabilities to environmental change This is true among organisms with free-living stages that differ in ploidy (e.g. algae, ferns; [11]). Our goal is to provide a generalized conceptual and novel experimental framework that can be used broadly across eukaryotes and importantly, is not restricted by taxon or by the specific details of the life cycle (box 1). These goals build upon [17], which considered similar questions from a quantitative genomic perspective. We explore the value of genomic analysis of single-generation artificial selection experiments because they can provide direct evidence of genetic correlations ( pleiotropy) in terms of allele frequencies, potentially minimizing the confounding ambiguities generated from environmental effects

Complex life cycles: an overview

Conceptual framework

Hypothesis-testing using genomics

Experimental design for detecting withingeneration selection

Power analysis

Alternative experimental genomic approaches

Study system considerations

Conclusion