Search for: All records

ABSTRACT Evolutionary genomic approaches provide powerful tools to understand variation in and evolution of physiological processes. Untargeted genomic or transcriptomic screens can identify functionally annotated candidate genes linked to specific physiological processes, in turn suggesting evolutionary roles for these processes. Such studies often aim to inform modeling of the potential of natural populations to adapt to climate change, but these models are most accurate when evolutionary responses are repeatable, and thus predictable. Here, we synthesize the evolutionary genetic and comparative transcriptomic literature on terrestrial and marine invertebrates to assess whether evolutionary responses to temperature are repeatable within populations, across populations and across species. There is compelling evidence for repeatability, sometimes even across species. However, responses to laboratory selection and geographic variation across thermal gradients appear to be highly idiosyncratic. We also survey whether genetic/transcriptomic studies repeatedly identify candidate genes in three functional groups previously associated with the response to thermal stress: heat shock protein (Hsp) genes, proteolysis genes and immunity genes. Multiple studies across terrestrial and marine species identify candidates included in these gene sets. Yet, each of the gene sets are identified in only a minority of studies. Together, these patterns suggest that there is limited predictability of evolutionary responses to natural selection, including across studies within species. We discuss specific patterns for the candidate gene sets, implications for predictive modeling, and other potential applications of evolutionary genetics in elucidating physiology and gene function. Finally, we discuss limitations of inferences from available evolutionary genetic studies and directions for future research. 

Abstract The bark beetle Ips typographus is the most destructive insect pest in Norway spruce-dominated forests. Its potential to establish multiple generations per year (multivoltinism) is one major trait that makes this beetle a severe pest. Ips typographus enters diapause to adjust its life cycle to seasonally changing environments. Diapause is characterized by developmental and reproductive arrest; it prolongs generation time and thus affects voltinism. In I. typographus a facultative, photoperiod-regulated diapause in the adult stage has been described. In addition, the presence of an obligate, photoperiod-independent, diapause has been hypothesized. The diapause phenotype has important implications for I. typographus voltinism, as populations with obligate diapausing individuals would be univoltine. To test for the presence of different I. typographus diapause phenotypes, we exposed Central and Northern European individuals to a set of photoperiodic treatments. We used two ovarian traits (egg number and vitellarium size) that are associated with gonad development, to infer reproductive arrest and thus diapause. We found a distinct effect of photoperiod on ovarian development, with variable responses in Central and Northern European beetles. We observed obligate diapausing (independent of photoperiod) individuals in Northern Europe, and both facultative (photoperiod-regulated) as well as obligate diapausing individuals in Central Europe. Our results show within-species variation for diapause induction, an adaptation to match life cycles with seasonally fluctuating environmental conditions. As the diapause phenotype affects the potential number of generations per season, our data are the basis for assessing the risk of outbreaks of this destructive bark beetle. 

ABSTRACT Organisms with complex life cycles demonstrate a remarkable ability to change their phenotypes across development, presumably as an evolutionary adaptation to developmentally variable environments. Developmental variation in environmentally sensitive performance, and thermal sensitivity in particular, has been well documented in holometabolous insects. For example, thermal performance in adults and juvenile stages exhibit little genetic correlation (genetic decoupling) and can evolve independently, resulting in divergent thermal responses. Yet, we understand very little about how this genetic decoupling occurs. We tested the hypothesis that genetic decoupling of thermal physiology is driven by fundamental differences in physiology between life stages, despite a potentially conserved cellular stress response. We used RNAseq to compare transcript expression in response to a cold stressor in Drosophila melanogaster larvae and adults and used RNA interference (RNAi) to test whether knocking down nine target genes differentially affected larval and adult cold tolerance. Transcriptomic responses of whole larvae and adults during and following exposure to −5°C were largely unique both in identity of responding transcripts and in temporal dynamics. Further, we analyzed the tissue-specificity of differentially expressed transcripts from FlyAtlas 2 data, and concluded that stage-specific differences in transcription were not simply driven by differences in tissue composition. In addition, RNAi of target genes resulted in largely stage-specific and sometimes sex-specific effects on cold tolerance. The combined evidence suggests that thermal physiology is largely stage-specific at the level of gene expression, and thus natural selection may be acting on different loci during the independent thermal adaptation of different life stages. 

Studies assessing the predictability of evolution typically focus on short-term adaptation within populations or the repeatability of change among lineages. A missing consideration in speciation research is to determine whether natural selection predictably transforms standing genetic variation within populations into differences between species. Here, we test whether and how host-related selection on diapause timing associates with genome-wide differentiation during ecological speciation by comparing ancestral hawthorn and newly formed apple-infesting host races of Rhagoletis pomonella to their sibling species Rhagoletis mendax that attacks blueberries. The associations of 57 857 single nucleotide polymorphisms in a diapause genome-wide-association study (GWAS) on the hawthorn race strongly predicted the direction and magnitude of genomic divergence among the three fly populations at a field site in Fennville, MI, USA. The apple race and R. mendax show parallel changes in the frequencies of putative inversions on three chromosomes associated with the earlier fruiting times of apples and blueberries compared to hawthorns. A diapause GWAS on R. mendax revealed compensatory changes throughout the genome accounting for the earlier eclosion of blueberry, but not apple flies. Thus, a degree of predictability, although not complete, exists in the genomics of diapause across the ecological speciation continuum in Rhagoletis . The generality of this result is placed in the context of other similar systems. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'. 

Many organisms enter a dormant state in their life cycle to deal with predictable changes in environments over the course of a year. The timing of dormancy is therefore a key seasonal adaptation, and it evolves rapidly with changing environments. We tested the hypothesis that differences in the timing of seasonal activity are driven by differences in the rate of development during diapause in Rhagoletis pomonella , a fly specialized to feed on fruits of seasonally limited host plants. Transcriptomes from the central nervous system across a time series during diapause show consistent and progressive changes in transcripts participating in diverse developmental processes, despite a lack of gross morphological change. Moreover, population genomic analyses suggested that many genes of small effect enriched in developmental functional categories underlie variation in dormancy timing and overlap with gene sets associated with development rate in Drosophila melanogaster . Our transcriptional data also suggested that a recent evolutionary shift from a seasonally late to a seasonally early host plant drove more rapid development during diapause in the early fly population. Moreover, genetic variants that diverged during the evolutionary shift were also enriched in putative cis regulatory regions of genes differentially expressed during diapause development. Overall, our data suggest polygenic variation in the rate of developmental progression during diapause contributes to the evolution of seasonality in R. pomonella . We further discuss patterns that suggest hourglass-like developmental divergence early and late in diapause development and an important role for hub genes in the evolution of transcriptional divergence.