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.

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.

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.

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.

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.

Environmentally induced development costs underlie fitness tradeoffs.

Local adaptation can lead to genotype-by-environment interactions, which can create fitness tradeoffs in alternative environments, and govern the distribution of biodiversity across geographic landscapes. Exploring the ecological circumstances that promote the evolution of fitness tradeoffs requires identifying how natural selection operates and during which ontogenetic stages natural selection is strongest. When organisms disperse to areas outside their natural range, tradeoffs might emerge when organisms struggle to reach key life history stages, or alternatively, die shortly after reaching life history stages if there are greater risks of mortality associated with costs to developing in novel environments. We used multiple populations from four ecotypes of an Australian native wildflower (Senecio pinnatifolius) in reciprocal transplants to explore how fitness tradeoffs arise across ontogeny. We then assessed whether the survival probability for plants from native and foreign populations was contingent on reaching key developmental stages. We found that fitness tradeoffs emerged as ontogeny progressed when native plants were more successful than foreign plants at reaching seedling establishment and maturity. Native and foreign plants that failed to reach seedling establishment died at the same rate, but plants from foreign populations died quicker than native plants after reaching seedling establishment, and died quicker regardless of whether they reached sexual maturity or not. Development rates were similar for native and foreign populations, but changed depending on the environment. Together, our results suggest that natural selection for environment-specific traits early in life history created tradeoffs between contrasting environments. Plants from foreign populations were either unable to develop to seedling establishment, or they suffered increased mortality as a consequence of reaching seedling establishment. The observation of tradeoffs together with environmentally dependent changes in development rate suggest that foreign environments induce organisms to develop at a rate different from their native habitat, incurring consequences for lifetime fitness and population divergence.

Diversification across a heterogeneous landscape.

Adaptation to contrasting environments across a heterogeneous landscape favors the formation of ecotypes by promoting ecological divergence. Patterns of fitness variation in the field can show whether natural selection drives local adaptation and ecotype formation. However, to demonstrate a link between ecological divergence and speciation, local adaptation must have consequences for reproductive isolation. Using contrasting ecotypes of an Australian wildflower, Senecio lautus in common garden experiments, hybridization experiments, and reciprocal transplants, we assessed how the environment shapes patterns of adaptation and the consequences of adaptive divergence for reproductive isolation. Local adaptation was strong between ecotypes, but weaker between populations of the same ecotype. F1 hybrids exhibited heterosis, but crosses involving one native parent performed better than those with two foreign parents. In a common garden experiment, F2 hybrids exhibited reduced fitness compared to parentals and F1 hybrids, suggesting that few genetic incompatibilities have accumulated between populations adapted to contrasting environments. Our results show how ecological differences across the landscape have created complex patterns of local adaptation and reproductive isolation, suggesting that divergent natural selection has played a fundamental role in the early stages of species diversification.

Convergence and divergence during the adaptation to similar environments by an Australian groundsel.

Adaptation to replicate environments is often achieved through similar phenotypic solutions. Whether selection also produces convergent genomic changes in these situations remains largely unknown. The variable groundsel, Senecio lautus, is an excellent system to investigate the genetic underpinnings of convergent evolution, because morphologically similar forms of these plants have adapted to the same environments along the coast of Australia. We compared range-wide patterns of genomic divergence in natural populations of this plant and searched for regions putatively affected by natural selection. Our results indicate that environmental adaptation followed complex genetic trajectories, affecting multiple loci, implying both the parallel recruitment of the same alleles and the divergence of completely different genomic regions across geography. An analysis of the biological functions of candidate genes suggests that adaptation to coastal environments may have occurred through the recruitment of different genes participating in similar processes. The relatively low genetic convergence that characterizes the parallel evolution of S. lautus forms suggests that evolution is more constrained at higher levels of biological organization.