From whole bodies to single cells: A guide to transcriptomic approaches for ecology and evolutionary biology.

RNA sequencing (RNAseq) methodology has experienced a burst of technological developments in the last decade, which has opened up opportunities for studying the mechanisms of adaptation to environmental factors at both the organismal and cellular level. Selecting the most suitable experimental approach for specific research questions and model systems can, however, be a challenge and researchers in ecology and evolution are commonly faced with the choice of whether to study gene expression variation in whole bodies, specific tissues, and/or single cells. A wide range of sometimes polarised opinions exists over which approach is best.

Germline proliferation trades off with lipid metabolism in .

Little is known about the metabolic basis of life-history trade-offs but lipid stores seem to play a pivotal role. During reproduction, an energetically highly costly process, animals mobilize fat reserves. Conversely, reduced or curtailed reproduction promotes lipid storage in many animals.

Microbes are potential key players in the evolution of life histories and aging in .

Microbes can have profound effects on host fitness and health and the appearance of late-onset diseases. Host-microbe interactions thus represent a major environmental context for healthy aging of the host and might also mediate trade-offs between life-history traits in the evolution of host senescence. Here, we have used the nematode to study how host-microbe interactions may modulate the evolution of life histories and aging.

An Ancestral Balanced Inversion Polymorphism Confers Global Adaptation.

Since the pioneering work of Dobzhansky in the 1930s and 1940s, many chromosomal inversions have been identified, but how they contribute to adaptation remains poorly understood. In Drosophila melanogaster, the widespread inversion polymorphism In(3R)Payne underpins latitudinal clines in fitness traits on multiple continents. Here, we use single-individual whole-genome sequencing, transcriptomics, and published sequencing data to study the population genomics of this inversion on four continents: in its ancestral African range and in derived populations in Europe, North America, and Australia.

The remoulding of dietary effects on the fecundity / longevity trade-off in a social insect.

Background: In many organisms increased reproductive effort is associated with a shortened life span. This trade-off is reflected in conserved molecular pathways that link nutrient-sensing with fecundity and longevity. Social insect queens apparently defy the fecundity / longevity trade-off as they are both, extremely long-lived and highly fecund.

A Single Nucleotide Variant in the PPARγ-homolog Eip75B Affects Fecundity in Drosophila.

Single nucleotide polymorphisms are the most common type of genetic variation, but how these variants contribute to the adaptation of complex phenotypes is largely unknown. Experimental evolution and genome-wide association studies have demonstrated that variation in the PPARγ-homolog Eip75B has associated with longevity and life-history differences in the fruit fly Drosophila melanogaster. Using RNAi knockdown, we first demonstrate that reduced expression of Eip75B in adult flies affects lifespan, egg-laying rate, and egg volume.

Natural alleles at the locus underpin evolutionary changes in lifespan and fecundity.

'Evolve and resequence' (E&R) studies in have identified many candidate loci underlying the evolution of ageing and life history, but experiments that validate the effects of such candidates remain rare. In a recent E&R study we have identified several alleles of the LAMMER kinase () as candidates for evolutionary changes in lifespan and fecundity. Here, we use two complementary approaches to confirm a functional role of in life-history evolution.

Genomic architecture of supergenes: connecting form and function.

Supergenes are tightly linked sets of loci that are inherited together and control complex phenotypes. While classical supergenes-governing traits such as wing patterns in butterflies or heterostyly in -have been studied since the Modern Synthesis, we still understand very little about how they evolve and persist in nature. The genetic architecture of supergenes is a critical factor affecting their evolutionary fate, as it can change key parameters such as recombination rate and effective population size, potentially redirecting molecular evolution of the supergene in addition to the surrounding genomic region.

Mutation accumulation opposes polymorphism: supergenes and the curious case of balanced lethals.

Supergenes offer spectacular examples of long-term balancing selection in nature, but their origin and maintenance remain a mystery. Reduced recombination between arrangements, a critical aspect of many supergenes, protects adaptive multi-trait phenotypes but can lead to mutation accumulation. Mutation accumulation can stabilize the system through the emergence of associative overdominance (AOD), destabilize the system, or lead to new evolutionary outcomes.

The rapid tempo of adaptation.

Selection in fruit flies leads to fast adaption to seasonal changes.

Transcriptomic evidence for a trade-off between germline proliferation and immunity in .

Life-history theory posits that investment into reproduction might occur at the expense of investment into somatic maintenance, including immune function. If so, reduced or curtailed reproductive effort might be expected to increase immunity. In support of this notion, work in has shown that worms lacking a germline exhibit improved immunity, but whether the antagonistic relation between germline proliferation and immunity also holds for other organisms is less well understood.

The Biology of Aging in Insects: From to Other Insects and Back.

An enormous amount of work has been done on aging in , a classical genetic and molecular model system, but also in numerous other insects. However, these two extensive bodies of work remain poorly integrated to date. Studies in often explore genetic, developmental, physiological, and nutrition-related aspects of aging in the lab, while studies in other insects often explore ecological, social, and somatic aspects of aging in both lab and natural populations.

Drosophila Evolution over Space and Time (DEST): A New Population Genomics Resource.

Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome data sets from natural populations of this species have been published over the last years. A major challenge is the integration of disparate data sets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D.

The discovery, distribution, and diversity of DNA viruses associated with in Europe.

is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described from the family Drosophilidae. This deficiency limits our opportunity to use natural host-pathogen combinations in experimental studies, and may bias our understanding of the virome. Here, we report fourteen DNA viruses detected in a metagenomic analysis of 6668 pool-sequenced , sampled from forty-seven European locations between 2014 and 2016.

On the fixation or nonfixation of inversions under epistatic selection.

Several recent publications have stated that epistatic fitness interactions cause the fixation of inversions that suppress recombination among the loci involved. Under this type of selection, however, the suppression of recombination in an inversion heterozygote can create a form of heterozygote advantage, which prevents the inversion from becoming fixed by selection. This process has been explicitly modelled by previous workers.

Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in .

To advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel among populations. Specifically, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identified parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations.

Gene Coexpression Network Reveals Highly Conserved, Well-Regulated Anti-Ageing Mechanisms in Old Ant Queens.

Evolutionary theories of ageing predict a reduction in selection efficiency with age, a so-called "selection shadow," due to extrinsic mortality decreasing effective population size with age. Classic symptoms of ageing include a deterioration in transcriptional regulation and protein homeostasis. Understanding how ant queens defy the trade-off between fecundity and lifespan remains a major challenge for the evolutionary theory of ageing.

Allelic polymorphism at foxo contributes to local adaptation in Drosophila melanogaster.

The insulin/insulin-like growth factor signalling pathway has been hypothesized as a major determinant of life-history profiles that vary adaptively in natural populations. In Drosophila melanogaster, multiple components of this pathway vary predictably with latitude; this includes foxo, a conserved gene that regulates insulin signalling and has pleiotropic effects on a variety of fitness-associated traits. We hypothesized that allelic variation at foxo contributes to genetic variance for size-related traits that vary adaptively with latitude.

Comparative transcriptomic analysis of the mechanisms underpinning ageing and fecundity in social insects.

The exceptional longevity of social insect queens despite their lifelong high fecundity remains poorly understood in ageing biology. To gain insights into the mechanisms that might underlie ageing in social insects, we compared gene expression patterns between young and old castes (both queens and workers) across different lineages of social insects (two termite, two bee and two ant species). After global analyses, we paid particular attention to genes of the insulin/insulin-like growth factor 1 signalling (IIS)/target of rapamycin (TOR)/juvenile hormone (JH) network, which is well known to regulate lifespan and the trade-off between reproduction and somatic maintenance in solitary insects.

Asymmetry, division of labour and the evolution of ageing in multicellular organisms.

Between the 1930s and 1960s, evolutionary geneticists worked out the basic principles of why organisms age. Despite much progress in the evolutionary biology of ageing since that time, however, many puzzles remain. The perhaps most fundamental of these is the question of which organisms should exhibit senescence and which should not (or which should age rapidly and which should not).

Genomic Analysis of European Drosophila melanogaster Populations Reveals Longitudinal Structure, Continent-Wide Selection, and Previously Unknown DNA Viruses.

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster.

Evolutionary genomics can improve prediction of species' responses to climate change.

Global climate change (GCC) increasingly threatens biodiversity through the loss of species, and the transformation of entire ecosystems. Many species are challenged by the pace of GCC because they might not be able to respond fast enough to changing biotic and abiotic conditions. Species can respond either by shifting their range, or by persisting in their local habitat.

Life-History Evolution and the Genetics of Fitness Components in .

Life-history traits or "fitness components"-such as age and size at maturity, fecundity and fertility, age-specific rates of survival, and life span-are the major phenotypic determinants of Darwinian fitness. Analyzing the evolution and genetics of these phenotypic targets of selection is central to our understanding of adaptation. Due to its simple and rapid life cycle, cosmopolitan distribution, ease of maintenance in the laboratory, well-understood evolutionary genetics, and its versatile genetic toolbox, the "vinegar fly" is one of the most powerful, experimentally tractable model systems for studying "life-history evolution.

Distinct genomic signals of lifespan and life history evolution in response to postponed reproduction and larval diet in .

Reproduction and diet are two major factors controlling the physiology of aging and life history, but how they interact to affect the evolution of longevity is unknown. Moreover, although studies of large-effect mutants suggest an important role of nutrient sensing pathways in regulating aging, the genetic basis of evolutionary changes in lifespan remains poorly understood. To address these questions, we analyzed the genomes of experimentally evolved populations subjected to a factorial combination of two selection regimes: reproductive age (early versus postponed), and diet during the larval stage ("low," "control," "high"), resulting in six treatment combinations with four replicate populations each.