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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. Expected final online publication date for the

Parallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origin of ecotypes is often inferred on the basis of a phylogeny which 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 is 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 inS. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.

Significance New species originate as populations become reproductively isolated from one another. Despite recent progress in uncovering the genetic basis of reproductive isolation, it remains unclear whether intrinsic reproductive barriers, such as hybrid sterility, can evolve as a by-product of local adaptation to contrasting environments. Here, we show that differences in a plant’s response to the pull of gravity have repeatedly evolved amongst coastal populations of an Australian wildflower, thus implicating a role of natural selection in their evolution. We found a strong genetic association between variation in this adaptive trait and hybrid sterility, suggesting that intrinsic reproductive barriers contribute to the origin of new species as populations adapt to heterogeneous environments., 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.

When organisms face similar ecological conditions, they often evolve similar phenotypic solutions. When this occurs independently and repeatedly in closely related taxa, it is referred to as parallel evolution. The correlation that arises between phenotype and environment in systems of parallelism provides some of the most compelling evidence for the role of natural selection in driving evolution. This is because it is unlikely that similar phenotypes would have evolved purely by chance. Systems of parallel evolution can thus be viewed as natural replicates of the evolutionary process, enabling researchers to study the genetics and ecology of how adaptation proceeds in nature. However, we still lack a comprehensive understanding of the processes that govern parallel divergence within natural systems, including how demographic history affects the likelihood of parallel evolution, how the extent of genotypic parallelism manifests at the level of the phenotype, and how divergent selection operates across multiple instances of repeated evolution. Here, I use the Australian wildflower species complex, Senecio lautus, as an emerging model system to study the dynamics of repeated evolution within nature. I focus on the Dune and Headland ecotypes of S. lautus, which inhabit contrasting environments along the coast of Australia and often occur in parapatry.I first provide an in-depth discussion of the field of parallel evolution in Chapter I. In Chapter II I demonstrate that S. lautus Dune and Headland populations have evolved multiple times independently. Using genotyping-by-sequencing data I observed phylogenetic clustering by geography, with strong genetic structure between populations, isolation by distance, and surprisingly minimal gene flow between parapatric pairs, as well as in the system as a whole. I further confirmed this analytically by demonstrating that gene flow is not high enough in S. lautus to obscure the observed phylogenetic relationships between populations. My work also highlights the necessity for researchers of parallel evolution to directly demonstrate that populations with similar adaptive phenotypes have evolved multiple independent times, which is surprisingly lacking in studies of parallel evolution. Next, in Chapter III I further contribute to the field of parallel evolution by creating a framework to quantify both genotypic and phenotypic parallelism within empirical systems. My framework is applicable to non-model organisms and provides a common set of analyses to measure parallel evolution. Using this framework, I demonstrate that S. lautus populations inhabiting similar environments have evolved strikingly similar phenotypes. However, these phenotypes have arisen via different mutational changes in different genes, although most contribute to the same biological functions. This suggests that adaptation within S. lautus might be constrained at the level of the biological function, where replicate populations have recruited different mutations in different genes. In Chapter IV I characterise the genomic landscape of parallel divergence across replicate populations within the system. I observed that genomic landscapes were highly heterogeneous, and populations that were more closely related contained landscapes that were more similar, which is consistent with the random accumulation of changes due to genetic drift. Surprisingly, divergent loci did not reside within regions of reduced recombination, and there was no evidence for a pervasive role of linked selection in shaping the observed genomic landscapes within S. lautus. I also identified a highly parallel region that is a candidate barrier locus thought to be resistant to gene flow and involved in the initial stages of population divergence. Finally in Chapter V, I summarise the findings of my three data chapters and provide future directions for the fields of parallel evolution and population genetics.Overall, my work has furthered our understanding of natural selection in the repeated evolution of similar phenotypes within nature. My results pave the way for identifying the causal genes for adaptation by directly linking them to adaptive phenotypes and further demonstrating that these phenotypes confer a fitness advantage within natural populations. Ultimately, my work allows us to begin to understand whether evolution within nature is repeatable and predictable.

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. This work was supported by an Australian Research Council grant (DP190103039) to DO and JE, and a University of Queensland Graduate School International Travel Award to MEJ

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 within 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 highlightsS. lautusas one of the most striking cases of phenotypic parallel evolution in nature.

In a number of animal species, divergent natural selection has repeatedly and independently driven the evolution of reproductive isolation between populations adapted to contrasting, but not to similar environments1. This process is known as parallel ecological speciation, and examples in plants are enigmatically rare2. Here, we perform a comprehensive test of the ecological speciation hypothesis in an Australian wildflower where parapatric populations found in coastal sand dunes (Dune ecotype) and headlands (Headland ecotype) have repeatedly and independently diverged in growth habit. Consistent with a role for divergent natural selection driving the evolution of reproductive isolation, we found that Dune populations with erect growth habit were easy to transplant across sand dunes, were largely interfertile despite half-a-million years of divergence, and were reproductively isolated from equally divergent Headland populations with prostrate growth habit. However, we unexpectedly discovered that both extrinsic and intrinsic reproductive isolation has evolved between prostrate Headland populations, suggesting that populations evolving convergent phenotypes can also rapidly become new species. Mutation-order speciation2, where the random accumulation of adaptive alleles create genetic incompatibilities between populations inhabiting similar habitats, provides a compelling explanation for these complex patterns of reproductive isolation. Our results suggest that natural selection can drive speciation effectively, but environmental and genetic complexity might make parallel ecological speciation uncommon in plants despite strong morphological convergence.

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.

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.

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.

The effects of high-low (HL) and low-high (LH) patterns of nutrition during the 5 weeks prior to a synchronized mating were studied on the reproductive performance of 115 Welsh Mountain and 114 Brecknock Cheviot ewes in a range of body condition at the start of treatment. For 2 months prior to treatment imposition, ewes were grazed in a systematic way at different stocking rates on different sward heights to obtain a range of body condition scores. Target score groupings were 2·00 to 2·25, 2·50 to 2·75 and 3·00 to 3·25 and although scores of 1·50 to 3·25 were obtained, most lay in the 2·00 to 2·75 range. Two treatment groups, balanced for live weight and body condition score, received high and low levels of nutrition for 16 days from mid October, achieved, respectively, by a low stocking rate on a sward with a high surface height plus ad libitum concentrate and a high stocking rate on a sward with a low surface height plus 200 g hay per head per day. Treatments were then reversed for the 17 days prior to mating. Live-weight and body condition-score changes were recorded and reproductive performance at first mating was measured from counts of corpora lutea and viable embryos at slaughter either at return to service or at 4 weeks after first mating. There were no differences due to nutritional pattern in live weight or body condition score at mating. The LH treatment significantly increased the rates of ovulation, conception, multiple ova survival and potential lambing per ewe pregnant and per ewe mated in the Welsh Mountain breed but significantly increased only the rates of ovulation and potential lambing per ewe pregnant in the Brecknock Cheviot breed compared with the HL treatment. The relatively poorer response in the latter breed was partially due to a lower ovulation rate potential coupled with non-significantly lower rates of conception and survival of single-shed ova associated with the LH treatment. Much of this relatively poorer reproductive performance in the Brecknock Cheviot breed was in ewes with body condition scores 3= 2·75. Reproductive performance increased with increasing body condition at the start of treatment over the range of scores =≤ 2·25 to 2·50 in both breeds and, while continuing to improve in scores above 2·50 in the Welsh Mountain breed, in the Brecknock Cheviot breed it started to decline. Ewes with a body condition score of 2·50 in both breeds showed the greatest response in potential lambing rate to the LH treatment.

In a 2 × 2 × 2 × 2 factorial experiment, the effects on reproductive performance of active immunization against androstenedione and of two sward heights in two periods, August to October (period 1) and October to November (period 2), were investigated in 144 Beulah Speckled-face and 146 Brecknock Cheviot ewes. Sward heights of either 5 to 6 cm (2200 kg dry matter (DM) per ha) (high) or 2 to 3 cm (650 kg DM per ha) (low) were achieved by adjustment of stocking rate during period 1. Two groups of ewes were balanced for body condition score across breed and sward height and the ewes of one group were actively immunized against androstenedione by injection with Fecundin® at 8 and 5 weeks before mating at the second synchronized oestrus after progestagen pessary withdrawal. Ewes were reallocated to the high (at 15 ewes per ha) and low (at 20 ewes per ha) swards at the start of period 2 by breed and immunization treatment, balanced for live weight, body condition score and sward height in period 1. After mating in mid November, all ewes were run at 19 ewes per ha on the residual pasture of the high sward until slaughtered either at return to service or at 4 weeks after first mating when corpora lutea and embryos were counted.There were no effects or interactions due to sward height in period 1 on the reproductive responses to sward height in period 2. Ovulation and potential lambing rates were greater in the Beulah breed than in the Cheviot, and on the high sward than on the low in period 2. Ovulation rates were higher in immunized ewes than in control ewes but the effects of immunization and sward height on potential lambing rate were not independent. Potential lambing rates were higher in immunized ewes than in control ewes at the low sward height but not at the high sward height.Adjustment of stocking rate during period 1 served to increase the range in ewe body condition at the start of period 2 in mid October. Reproductive response to body condition at this time differed between the breeds, the relationship being strongly positive in the more prolific Beulah control ewes but less so in the less prolific Cheviot control ewes. The response to immunization in both breeds was relatively greater at lower levels of body condition, thereby reducing the effect of body condition in immunized ewes.The use of Fecundin® is therefore unlikely to produce much advantage when pre-mating nutrition or body condition are high but there may be some advantage in using it when nutritional resources are limited in the autumn, particularly in ewes in poorer body condition.