skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, October 10 until 2:00 AM ET on Friday, October 11 due to maintenance. We apologize for the inconvenience.


Title: Ecological mechanism of climate‐mediated selection in a rapidly evolving invasive species
Abstract

Recurring seasonal changes can lead to the evolution of phenological cues. For example, many arthropods undergo photoperiodic diapause, a programmed developmental arrest induced by short autumnal day length. The selective mechanisms that determine the timing of autumnal diapause initiation have not been empirically identified. We quantified latitudinal clines in genetically determined diapause timing of an invasive mosquito,Aedes albopictus,on two continents. We show that variation in diapause timing within and between continents is explained by a novel application of a growing degree day (GDD) model that delineates a location‐specific deadline after which it is not possible to complete an additional full life cycle. GDD models are widely used to predict spring phenology by modelling growth and development as physiological responses to ambient temperatures. Our results show that the energy accumulation dynamics represented by GDD models have also led to the evolution of an anticipatory life‐history cue in autumn.

 
more » « less
Award ID(s):
1702664
NSF-PAR ID:
10372669
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Ecology Letters
Volume:
24
Issue:
4
ISSN:
1461-023X
Page Range / eLocation ID:
p. 698-707
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Understanding the molecular basis of repeated evolution improves our ability to predict evolution across the tree of life. Only since the last decade has high‐throughput sequencing enabled comparative genome scans to thoroughly examine the repeatability of genetic changes driving repeated phenotypic evolution. The Asian corn borer (ACB),Ostrinia furnacalis(Guenée), and the European corn borer (ECB),Ostrinia nubilalis(Hübner), are two closely related moths displaying repeatable phenological adaptation to a wide range of climates on two separate continents, largely manifesting as changes in the timing of diapause induction and termination across latitude. Candidate genes underlying diapause variation in North American ECB have been previously identified. Here, we sampled seven ACB populations across 23 degrees of latitude in China to elucidate the genetic basis of diapause variation and evolutionary mechanisms driving parallel clinal responses in the two species. Using pooled whole‐genome sequencing (Pool‐seq) data, population genomic analyses revealed hundreds of single nucleotide polymorphisms (SNP) whose allele frequencies covaried with mean diapause phenotypes along the cline. Genes involved in circadian rhythm were over‐represented among candidate genes with strong signatures of spatially varying selection. Only one of two circadian clock genes associated with diapause evolution in ECB showed evidence of reuse in ACB (period [per]), butperalleles were not shared between species nor with their outgroup, implicating independent mutational paths. Nonetheless, evidence of adaptive introgression was discovered at putative diapause loci located elsewhere in the genome, suggesting that de novo mutations and introgression might both underlie the repeated phenological evolution.

     
    more » « less
  2. Abstract

    For insect species in temperate environments, seasonal timing is often governed by the regulation of diapause, a complex developmental programme that allows insects to weather unfavourable conditions and synchronize their life cycles with available resources. Diapause development consists of a series of distinct phases including initiation, maintenance, termination and post‐diapause development. The evolution of insect seasonal timing depends in part on how these phases of diapause development and post‐diapause development interact to affect variation in phenology. Here, we dissect the physiological basis of a recently evolved phenological shift inRhagoletis pomonella(Diptera: Tephritidae), a model system for ecological divergence. A recently derived population ofR. pomonellashifted from specializing on native hawthorn fruit to earlier fruiting introduced apples, resulting in a 3–4 week shift in adult emergence timing. We tracked metabolic rates of individual flies across post‐winter development to test which phases of development may act either independently or in combination to contribute to this recently evolved divergence in timing. Apple and hawthorn flies differed in a number of facets of their post‐winter developmental trajectories. However, divergent adaptation in adult emergence phenology in these flies was due almost entirely to the end of the pupal diapause maintenance phase, with post‐diapause development having a very small effect. The relatively simple underpinnings of variation in adult emergence phenology suggest that further adaptation to seasonal change in these flies for this trait might be largely due to the timing of diapause termination unhindered by strong covariance among different components of post‐diapause development.

     
    more » « less
  3. Premise

    Boreal and northern temperate forest trees possess finely tuned mechanisms of dormancy, which match bud phenology with local seasonality. After winter dormancy, the accumulation of chilling degree days (CDD) required for rest completion before the accumulation of growing degree days (GDD) during quiescence is an important step in the transition to spring bud flush. While bud flush timing is known to be genetically variable within species, few studies have investigated variation among genotypes from different climates in response to variable chilling duration.

    Methods

    We performed a controlled environment study using dormant cuttings from 10 genotypes ofPopulus balsamifera, representing a broad latitudinal gradient (43–58°N). We exposed cuttings to varying amounts of chilling (0–10 weeks) and monitored subsequent GDD to bud flush at a constant forcing temperature.

    Results

    Chilling duration strongly accelerated bud flush timing, with increasing CDD resulting in fewer GDD to flush. Genotypic variation for bud flush was significant and stratified by latitude, with southern genotypes requiring more GDD to flush than northern genotypes. The latitudinal cline was pronounced under minimal chilling, whereas genotypic variation in GDD to bud flush converged as CDD increased.

    Conclusions

    We demonstrate that increased chilling lessens GDD to bud flush in a genotype‐specific manner. Our results emphasize that latitudinal clines in bud flush reflect a critical genotype‐by‐environment interaction, whereby differences in bud flush between southern vs. northern genotypes depend on chilling. Our results suggest selection has shaped chilling requirements and depth of rest as an adaptive strategy to avoid precocious flush in climates with midwinter warming.

     
    more » « less
  4. Introduction

    Females of the Northern house mosquito,Culex pipiens, enter an overwintering dormancy, or diapause, in response to short day lengths and low environmental temperatures that is characterized by small egg follicles and high starvation resistance. During diapause,Culex pipiensMajor Royal Jelly Protein 1 ortholog (CpMRJP1) is upregulated in females ofCx. pipiens. This protein is highly abundant in royal jelly, a substance produced by honey bees (Apis mellifera), that is fed to future queens throughout larval development and induces the queen phenotype (e.g., high reproductive activity and longer lifespan). However, the role of CpMRJP1 inCx. pipiensis unknown.

    Methods

    We first conducted a phylogenetic analysis to determine how the sequence of CpMRJP1 compares with other species. We then investigated how supplementing the diets of both diapausing and nondiapausing females ofCx. pipienswith royal jelly affects egg follicle length, fat content, protein content, starvation resistance, and metabolic profile.

    Results

    We found that feeding royal jelly to females reared in long-day, diapause-averting conditions significantly reduced the egg follicle lengths and switched their metabolic profiles to be similar to diapausing females. In contrast, feeding royal jelly to females reared in short-day, diapause-inducing conditions significantly reduced lifespan and switched their metabolic profile to be similar nondiapausing mosquitoes. Moreover, RNAi directed againstCpMRJPIsignificantly increased egg follicle length of short-day reared females, suggesting that these females averted diapause.

    Discussion

    Taken together, our data show that consuming royal jelly reverses several key seasonal phenotypes ofCx. pipiensand that these responses are likely mediated in part by CpMRJP1.

     
    more » « less
  5. Abstract

    The monarch butterfly (Danaus plexippus) complements its iconic migration with diapause, a hormonally controlled developmental programme that contributes to winter survival at overwintering sites. Although timing is a critical adaptive feature of diapause, how environmental cues are integrated with genetically‐determined physiological mechanisms to time diapause development, particularly termination, is not well understood. In a design that subjected western North American monarchs to different environmental chamber conditions over time, we modularized constituent components of an environmentally‐controlled, internal diapause termination timer. Using comparative transcriptomics, we identified molecular controllers of these specific diapause termination components. Calcium signalling mediated environmental sensitivity of the diapause timer, and we speculate that it is a key integrator of environmental condition (cold temperature) with downstream hormonal control of diapause. Juvenile hormone (JH) signalling changed spontaneously in diapause‐inducing conditions, capacitating response to future environmental condition. Although JH is a major target of the internal timer, it is not itself the timer. Epigenetic mechanisms are implicated to be the proximate timing mechanism. Ecdysteroid, JH, and insulin/insulin‐like peptide signalling are major targets of the diapause programme used to control response to permissive environmental conditions. Understanding the environmental and physiological mechanisms of diapause termination sheds light on fundamental properties of biological timing, and also helps inform expectations for how monarch populations may respond to future climate change.

     
    more » « less