The genomic consequences of selection across development.

Understanding how natural selection drives diversification in nature has been at the forefront of biological research for over a century. The main idea is simple: natural selection favours individuals best suited to pass on their genes. However, the journey from birth to reproduction is complex as organisms experience multiple developmental stages, each influenced by genetic and environmental factors (Orr, 2009). These complexities compound even further as each stage of development might be governed by a unique underlying set of alleles and genes. In this issue of Molecular Ecology, Goebl et al. (2022) examine the role of natural selection in driving ecotypic divergence across different life history stages of the prairie sunflower Helianthus petiolaris. The authors used reciprocal transplant experiments, demographic models, and genomic sequencing to explore fitness variation across developmental stages. They show how natural selection impacts population divergence across multiple life history stages and evaluate the resulting allele frequency changes. Goebl et al. link these results to the role of chromosomal inversions, thus furthering our understanding of how ecological divergence proceeds in the face of gene flow. Below, we explore these results in detail and complement their interpretation by considering the evolution of genetic correlations amongst traits governing fitness.

The Ecology of Hybrid Incompatibilities.

Ecologically mediated selection against hybrids, caused by hybrid phenotypes fitting poorly into available niches, is typically viewed as distinct from selection caused by epistatic Dobzhansky-Muller hybrid incompatibilities. Here, we show how selection against transgressive phenotypes in hybrids manifests as incompatibility. After outlining our logic, we summarize current approaches for studying ecology-based selection on hybrids. We then quantitatively review QTL-mapping studies and find traits differing between parent taxa are typically polygenic. Next, we describe how verbal models of selection on hybrids translate to phenotypic and genetic fitness landscapes, highlighting emerging approaches for detecting polygenic incompatibilities. Finally, in a synthesis of published data, we report that trait transgression-and thus possibly extrinsic hybrid incompatibility in hybrids-escalates with the phenotypic divergence between parents. We discuss conceptual implications and conclude that studying the ecological basis of hybrid incompatibility will facilitate new discoveries about mechanisms of speciation.

Hypergraphs and centrality measures identifying key features in gene expression data.

Multidisciplinary approaches can significantly advance our understanding of complex systems. For instance, gene co-expression networks align prior knowledge of biological systems with studies in graph theory, emphasising pairwise gene to gene interactions. In this paper, we extend these ideas, promoting hypergraphs as an investigative tool for studying multi-way interactions in gene expression data. Additional freedoms are achieved by representing individual genes with hyperedges, and simultaneously testing each gene against many features/vertices. Further gene/hyperedge interactions can be captured and explored using the line graph representations, a technique that reduces the complexity of dense hypergraphs. Such an approach provides access to graph centrality measures, which identifies salient features within a data set. For instance dominant or hub-like hyperedges, leading to key knowledge on gene expression. The validity of this approach is established through the study of gene expression data for the plant species Senecio lautus and results will be interpreted within this biological setting.

Uncovering the genetic architecture of parallel evolution.

Identifying the genetic architecture underlying adaptive traits is exceptionally challenging in natural populations. This is because associations between traits not only mask the targets of selection but also create correlated patterns of genomic divergence that hinder our ability to isolate causal genetic effects. Here, we examine the repeated evolution of components of the auxin pathway that have contributed to the replicated loss of gravitropism (i.e. the ability of a plant to bend in response to gravity) in multiple populations of the Senecio lautus species complex in Australia. We use a powerful approach which combines parallel population genomics with association mapping in a Multiparent Advanced Generation Inter-Cross (MAGIC) population to break down genetic and trait correlations to reveal how adaptive traits evolve during replicated evolution. We sequenced auxin and shoot gravitropism-related gene regions in 80 individuals from six natural populations (three parallel divergence events) and 133 individuals from a MAGIC population derived from two of the recently diverged natural populations. We show that artificial tail selection on gravitropism in the MAGIC population recreates patterns of parallel divergence in the auxin pathway in the natural populations. We reveal a set of 55 auxin gene regions that have evolved repeatedly during the evolution of the species, of which 50 are directly associated with gravitropism divergence in the MAGIC population. Our work creates a strong link between patterns of genomic divergence and trait variation contributing to replicated evolution by natural selection, paving the way to understand the origin and maintenance of adaptations in natural populations.

Crop adaptation to climate change: An evolutionary perspective.

The disciplines of evolutionary biology and plant and animal breeding have been intertwined throughout their development, with responses to artificial selection yielding insights into the action of natural selection and evolutionary biology providing statistical and conceptual guidance for modern breeding. Here we offer an evolutionary perspective on a grand challenge of the 21st century: feeding humanity in the face of climate change. We first highlight promising strategies currently under way to adapt crops to current and future climate change. These include methods to match crop varieties with current and predicted environments and to optimize breeding goals, management practices, and crop microbiomes to enhance yield and sustainable production. We also describe the promise of crop wild relatives and recent technological innovations such as speed breeding, genomic selection, and genome editing for improving environmental resilience of existing crop varieties or for developing new crops. Next, we discuss how methods and theory from evolutionary biology can enhance these existing strategies and suggest novel approaches. We focus initially on methods for reconstructing the evolutionary history of crops and their pests and symbionts, because such historical information provides an overall framework for crop-improvement efforts. We then describe how evolutionary approaches can be used to detect and mitigate the accumulation of deleterious mutations in crop genomes, identify alleles and mutations that underlie adaptation (and maladaptation) to agricultural environments, mitigate evolutionary trade-offs, and improve critical proteins. Continuing feedback between the evolution and crop biology communities will ensure optimal design of strategies for adapting crops to climate change.

Replicated Evolution in Plants.

Similar traits and functions commonly evolve in nature. Here, we explore patterns of replicated evolution across the plant kingdom and discuss the processes responsible for such patterns. We begin this review by defining replicated evolution and the theoretical, genetic, and ecological concepts that help explain it. We then focus our attention on empirical cases of replicated evolution at the phenotypic and genotypic levels. We find that replication at the ecotype level is common, but evidence for repeated ecological speciation is surprisingly sparse. On the other hand, the replicated evolution of ecological strategies and physiological mechanisms across similar biomes appears to be pervasive. We conclude by highlighting where future efforts can help us bridge the understanding of replicated evolution across different levels of biological organization. Earth's landscape is diverse but also repeats itself. Organisms seem to have followed suit.

The influence of genetic structure on phenotypic diversity in the Australian mango (Mangifera indica) gene pool.

Genomic selection is a promising breeding technique for tree crops to accelerate the development of new cultivars. However, factors such as genetic structure can create spurious associations between genotype and phenotype due to the shared history between populations with different trait values. Genetic structure can therefore reduce the accuracy of the genotype to phenotype map, a fundamental requirement of genomic selection models. Here, we employed 272 single nucleotide polymorphisms from 208 Mangifera indica accessions to explore whether the genetic structure of the Australian mango gene pool explained variation in trunk circumference, fruit blush colour and intensity. Multiple population genetic analyses indicate the presence of four genetic clusters and show that the most genetically differentiated cluster contains accessions imported from Southeast Asia (mainly those from Thailand). We find that genetic structure was strongly associated with three traits: trunk circumference, fruit blush colour and intensity in M. indica. This suggests that the history of these accessions could drive spurious associations between loci and key mango phenotypes in the Australian mango gene pool. Incorporating such genetic structure in associations between genotype and phenotype can improve the accuracy of genomic selection, which can assist the future development of new cultivars.

Comparisons of chemosensory gene repertoires in human and non-human feeding Anopheles mosquitoes link olfactory genes to anthropophily.

We investigate the genetic basis of anthropophily (human host use) in a non-model mosquito species group, the Anopheles farauti complex from the southwest Pacific. This complex has experienced multiple transitions from anthropophily to zoophily, contrasting with well-studied systems (the global species Aedes aegypti and the African Anopheles gambiae complex) that have evolved to be specialist anthropophiles. By performing tests of selection and assessing evolutionary patterns for >200 olfactory genes from nine genomes, we identify several candidate genes associated with differences in anthropophily in this complex. Based on evolutionary patterns (phylogenetic relationships, fixed amino acid differences, and structural differences) as well as results from selection analyses, we identify numerous genes that are likely to play an important role in mosquitoes' ability to detect humans as hosts. Our findings contribute to the understanding of the evolution of insect olfactory gene families and mosquito host preference as well as having potential applied outcomes.

Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower.

Natural selection is responsible for much of the diversity we see in nature. Just as it drives the evolution of new traits, it can also lead to new species. However, it is unclear whether natural selection conferring adaptation to local environments can drive speciation through the evolution of hybrid sterility between populations. Here, we show that adaptive divergence in shoot gravitropism, the ability of a plant's shoot to bend upwards in response to the downward pull of gravity, contributes to the evolution of hybrid sterility in an Australian wildflower, Senecio lautus We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction using a hybrid population subjected to eight rounds of recombination and three rounds of selection in the field. Our experiments revealed that shoot gravitropism responds to natural selection in the expected direction of the locally adapted population. Using the advanced hybrid population, we discovered that individuals with extreme differences in gravitropism had more sterile crosses than individuals with similar gravitropic responses, which were largely fertile, indicating that this adaptive trait is genetically correlated with hybrid sterility. Our results suggest that natural selection can drive the evolution of locally adaptive traits that also create hybrid sterility, thus revealing an evolutionary connection between local adaptation and the origin of new species.

Gene flow between island populations of the malaria mosquito, Anopheles hinesorum, may have contributed to the spread of divergent host preference phenotypes.

Anopheles hinesorum is a mosquito species with variable host preference. Throughout New Guinea and northern Australia, An. hinesorum feeds on humans (it is opportunistically anthropophagic) while in the south-west Pacific's Solomon Archipelago, the species is abundant but has rarely been found biting humans (it is exclusively zoophagic in most populations). There are at least two divergent zoophagic (nonhuman biting) mitochondrial lineages of An. hinesorum in the Solomon Archipelago representing two independent dispersals. Since zoophagy is a derived (nonancestral) trait in this species, this leads to the question: has zoophagy evolved independently in these two populations? Or conversely: has nuclear gene flow or connectivity resulted in the transfer of zoophagy? Although we cannot conclusively answer this, we find close nuclear relationships between Solomon Archipelago populations indicating that recent nuclear gene flow has occurred between zoophagic populations from the divergent mitochondrial lineages. Recent work on isolated islands of the Western Province (Solomon Archipelago) has also revealed an anomalous, anthropophagic island population of An. hinesorum. We find a common shared mitochondrial haplotype between this Solomon Island population and another anthropophagic population from New Guinea. This finding suggests that there has been recent migration from New Guinea into the only known anthropophagic population from the Solomon Islands. Although currently localized to a few islands in the Western Province of the Solomon Archipelago, if anthropophagy presents a selective advantage, we may see An. hinesorum emerge as a new malaria vector in a region that is now working on malaria elimination.

Phenotypic and genotypic parallel evolution in parapatric ecotypes of Senecio.

The independent and repeated adaptation of populations to similar environments often results in the evolution of similar forms. This phenomenon creates a strong correlation between phenotype and environment and is referred to as parallel evolution. However, we are still largely unaware of the dynamics of parallel evolution, as well as the interplay between phenotype and genotype within natural systems. Here, we examined phenotypic and genotypic parallel evolution in multiple parapatric Dune-Headland coastal ecotypes of an Australian wildflower, Senecio lautus. We observed a clear trait-environment association in the system, with all replicate populations having evolved along the same phenotypic evolutionary trajectory. Similar phenotypes have arisen via mutational changes occurring in different genes, although many share the same biological functions. Our results shed light on how replicated adaptation manifests at the phenotypic and genotypic levels within populations, and highlight S. lautus as one of the most striking cases of phenotypic parallel evolution in nature.

Highly Replicated Evolution of Parapatric Ecotypes.

Parallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origins of ecotypes are often inferred based on a phylogeny that clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic because gene flow and incomplete lineage sorting can uncouple the genetic structure at neutral markers from the colonization history of populations. Here, we demonstrate multiple origins within ecotypes of an Australian wildflower, Senecio lautus. We observed strong genetic structure as well as phylogenetic clustering by geography and show that this is unlikely due to gene flow between parapatric ecotypes, which was surprisingly low. We further confirm this analytically by demonstrating that phylogenetic distortion due to gene flow often requires higher levels of migration than those observed in S. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.

Homage to Felsenstein 1981, or why are there so few/many species?

If there are no constraints on the process of speciation, then the number of species might be expected to match the number of available niches and this number might be indefinitely large. One possible constraint is the opportunity for allopatric divergence. In 1981, Felsenstein used a simple and elegant model to ask if there might also be genetic constraints. He showed that progress towards speciation could be described by the build-up of linkage disequilibrium among divergently selected loci and between these loci and those contributing to other forms of reproductive isolation. Therefore, speciation is opposed by recombination, because it tends to break down linkage disequilibria. Felsenstein then introduced a crucial distinction between "two-allele" models, which are subject to this effect, and "one-allele" models, which are free from the recombination constraint. These fundamentally important insights have been the foundation for both empirical and theoretical studies of speciation ever since.

Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation.

Adaptation to contrasting environments occurs when advantageous alleles accumulate in each population, but it remains largely unknown whether these same advantageous alleles create genetic incompatibilities that can cause intrinsic reproductive isolation leading to speciation. Identifying alleles that underlie both adaptation and reproductive isolation is further complicated by factors such as dominance and genetic interactions among loci, which can affect both processes differently and obscure potential links between adaptation and speciation. Here, we use a combination of field and glasshouse experiments to explore the connection between adaptation and speciation while accounting for dominance and genetic interactions. We created a hybrid population with equal contributions from four contrasting ecotypes of Senecio lautus (Asteraceae), which produced hybrid genomes both before (F1 hybrid generation) and after (F4 hybrid generation) recombination among the parental ecotypes. In the glasshouse, plants in the second generation (F2 hybrid generation) showed reduced fitness as a loss of fertility. However, fertility was recovered in subsequent generations, suggesting that genetic variation underlying the fitness reduction was lost in subsequent generations. To quantify the effects of losing genetic variation at the F2 generation on the fitness of later generation hybrids, we used a reciprocal transplant to test for fitness differences between parental ecotypes, and F1 and F4 hybrids in all four parental habitats. Compared to the parental ecotypes and F1 hybrids, variance in F4 hybrid fitness was lower, and lowest in habitats that showed stronger native-ecotype advantage, suggesting that stronger natural selection for the native ecotype reduced fitness variation in the F4 hybrids. Fitness trade-offs that were present in the parental ecotypes and F1 hybrids were absent in the F4 hybrid. Together, these results suggest that the genetic variation lost after the F2 generation was likely associated with both adaptation and intrinsic reproductive isolation among ecotypes from contrasting habitats.

Senecio as a model system for integrating studies of genotype, phenotype and fitness.

Two major developments have made it possible to use examples of ecological radiations as model systems to understand evolution and ecology. First, the integration of quantitative genetics with ecological experiments allows detailed connections to be made between genotype, phenotype, and fitness in the field. Second, dramatic advances in molecular genetics have created new possibilities for integrating field and laboratory experiments with detailed genetic sequencing. Combining these approaches allows evolutionary biologists to better study the interplay between genotype, phenotype, and fitness to explore a wide range of evolutionary processes. Here, we present the genus Senecio (Asteraceae) as an excellent system to integrate these developments, and to address fundamental questions in ecology and evolution. Senecio is one of the largest and most phenotypically diverse genera of flowering plants, containing species ranging from woody perennials to herbaceous annuals. These Senecio species exhibit many growth habits, life histories, and morphologies, and they occupy a multitude of environments. Common within the genus are species that have hybridized naturally, undergone polyploidization, and colonized diverse environments, often through rapid phenotypic divergence and adaptive radiation. These diverse experimental attributes make Senecio an attractive model system in which to address a broad range of questions in evolution and ecology.