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Evolution can repeat itself, resulting in parallel adaptations in independent lineages occupying similar environments. Moreover, parallel evolution sometimes, but not always, uses the same genes. Two main hypotheses have been put forth to explain the probability and extent of parallel evolution. First, parallel evolution is more likely when shared ecologies result in similar patterns of natural selection in different taxa. Second, parallelism is more likely when genomes are similar because of shared standing variation and similar mutational effects in closely related genomes. Here we combine ecological, genomic, experimental and phenotypic data with Bayesian modelling and randomization tests to quantify the degree of parallelism and its relationship with ecology and genetics. Our results show that the extent to which genomic regions associated with climate are parallel among species of Timema stick insects is shaped collectively by shared ecology and genomic background. Specifically, the extent of genomic parallelism decays with divergence in climatic conditions (that is, habitat or ecological similarity) and genomic similarity. Moreover, we find that climate-associated loci are likely subject to selection in a field experiment, overlap with genetic regions associated with cuticular hydrocarbon traits and are not strongly shaped by introgression between species. Our findings shed light on when evolution is most expected to repeat itself.

Additional methods and results

Tables S3 and S6; Figures S1-S3

A fastSTRUCTURE analysis based on all SNPs and for all populations of R. pomonella included in this study, considering K=2–6 subpopulations.

Correlation coefficients between SNP allele frequency differences in the hawthorn host race and R. mendax eclosion time GWAS for all polymorphic loci genotyped in the two taxa and those mapping to chromosomes 1–5. Probability (P) level determined by Monte-Carlo non-parametric computer simulations (n=10,000 replicates). n SNPs=number of SNPs in a given comparison.

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 R. mendax that attacks blueberries. The associations of 57 857 single nucleotide polymorphisms in a diapause genome-wide-association studies (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'.

Correlation coefficients (r) between SNP allele frequency differences in the R. mendax eclosion time GWAS versus the differences between R. mendax and the hawthorn host race (Blue-Haw) and R. mendax and the apple race (Blue-Ap) at the Fennville site. Results are given for all variable SNPs in the R. mendax eclosion study, as well as for loci mapping to chromosomes 1-5 and for high (H), medium (M), and low LD classes of loci on each chromosome (Chrome), as determined in Egan et al. (2015) and Ragland et al. (2017). Probability (P) levels determined by Monte-Carlo, non-parametric computer simulations (n=10,000 replicates), with significant relationships bolded. n SNPs=number SNPs in comparison.

Genomic correlation between eclosion variation and geographic differentiation in the R. pomonella hawthorn race in the Midwest USA, based on data from Ragland et al. (2017) and Doellman et al. (2019), and reanalyzed using the 44,749 SNPs called in this study. Scatterplots depict the relationship between the difference in allele frequency between late versus early eclosing samples of hawthorn flies (x-axis; eclosion time GWAS) and the difference in allele frequency between Urbana, Illinois (south) and Fennville, Michigan (north) study sites (y-axis; geographic cline). (A) graph for all SNPs genotyped in the study (r=0.446, PR. pomonella that has been hypothesized to take the form of clinal variation due to past geographic isolation, divergence, and secondary contact between hawthorn-infesting populations in Mexico and the USA (Feder et al. 2003).

Linkage disequilibrium (LD) network plots for SNPs mapping to chromosomes 1–5, demonstrating correspondence between high LD loci between R. pomonella and R. mendax. Loci are shown as nodes (circles) connected to one another in clusters by edges, when pairwise LD (r2) between loci exceeds 0.8. Tight clusters indicate this high pairwise LD between many SNPs, while unconnected SNPs have a pairwise LD below 0.8 with all other SNPs on the same chromosome. Within population LD is represented for the hawthorn host race of R. pomonella (panels A-E) and the blueberry-infesting population of R. mendax (panels F-J). Black circles represent high LD SNPs residing in the putative inversions segregating within R. pomonella. Note that on chromosomes 3 and 5, many of the SNPs in the high LD clusters in R. pomonella are also in high LD with one another in R. mendax. This suggests that the two species share large inversion polymorphisms on these two chromosomes.

Correlation coefficients (r) between SNP allele frequency differences in the hawthorn race eclosion time GWAS versus the differences between the apple and hawthorn host races (Ap-Haw) and R. mendax and the hawthorn race (Blue-Haw) at the Fennville site. Results are given for all variable SNPs in the hawthorn eclosion study, as well as for loci mapping to chromosomes 1–5 and for high (H), medium (M), and low LD classes of loci on each chromosome (Chrome), as determined in Egan et al. (2015) and Ragland et al. (2017). Probability (P) levels determined by Monte-Carlo, non-parametric computer simulations (n=10,000 replicates), with significant relationships bolded. n SNPs=number SNPs in comparison.

OSM 1: Additional information on Gambusia collection sites. (DOCX 2179Â kb)

Theory predicts that dispersal throughout metapopulations has a variety of consequences for the abundance and distribution of species. Immigration is predicted to increase abundance and habitat patch occupancy, but gene flow can have both positive and negative demographic consequences. Here, we address the eco-evolutionary effects of dispersal in a wild metapopulation of the stick insect Timema cristinae, which exhibits variable degrees of local adaptation throughout a heterogeneous habitat patch network of two host-plant species. To disentangle the ecological and evolutionary contributions of dispersal to habitat patch occupancy and abundance, we contrasted the effects of connectivity to populations inhabiting conspecific host plants and those inhabiting the alternate host plant. Both types of connectivity should increase patch occupancy and abundance through increased immigration and sharing of beneficial alleles through gene flow. However, connectivity to populations inhabiting the alternate host-plant species may uniquely cause maladaptive gene flow that counters the positive demographic effects of immigration. Supporting these predictions, we find the relationship between patch occupancy and alternate-host connectivity to be significantly smaller in slope than the relationship between patch occupancy and conspecific-host connectivity. Our findings illustrate the ecological and evolutionary roles of dispersal in driving the distribution and abundance of species.

Genetička arhitektura fenotipskih obilježja školjkaša, odnosno njihova nasljednost, broj uključenih lokusa i njihov učinak vrlo su slabo istraženi. Mijenjajući uvjete okoliša, antropogeno onečišćenje može putem inducirajućeg ili genotipskog učinka utjecati na morfologiju dagnje (Mytilus galloprovincialis). Da bismo procijenili genetičku arhitekturu morfologije dagnje mjerili smo 15 morfoloških obilježja na 1700 jedinki iz dviju populacija koje nastanjuju područja različitog stupnja onečišćenja. Koristeći sekvenciranje nove generacije sakupili smo mnogobrojne genomske podatke, te analizirali genetičku arhitekturu morfoloških obilježja pomoću metode genomske asocijacije GWAS (eng. genome-wide association study). Odredili smo i genetičku arhitekturu istih obilježja te procijenili fitnes za po 20 jedinki iz dodatnih 15 populacija s postaja različitog stupnja onečišćenja. Rezultati ovog istraživanja opisuju unutar i među-populacijsku varijabilnost u morfologiji dagnje te omogućuju uvid u interakciju između genotipa, fenotipa i okoliša.

Ecological speciation is the process by which barriers to gene flow between populations evolve due to adaptive divergence via natural selection. A relatively unexplored area in ecological speciation is the role of gene expression. Gene expression may be associated with ecologically important phenotypes not evident from morphology and play a role during colonization of new environments. Here we review two potential roles of gene expression in ecological speciation: (1) its indirect role in facilitating population persistence and (2) its direct role in contributing to genetically based reproductive isolation. We find indirect evidence that gene expression facilitates population persistence, but direct tests are lacking. We also find clear examples of gene expression having effects on phenotypic traits and adaptive genetic divergence, but links to the evolution of reproductive isolation itself remain indirect. Gene expression during adaptive divergence seems to often involve complex genetic architectures controlled by gene networks, regulatory regions, and "eQTL hotspots." Nonetheless, we review how approaches for isolating the functional mutations contributing to adaptive divergence are proving to be successful. The study of gene expression has promise for increasing our understanding ecological speciation, particularly when integrative approaches are applied.

Sympatric speciation remains controversial. 'Sympatry' originally meant "in the same geographical area", Recently, evolutionists have redefined 'sympatric speciation' non-spatially to require panmixia (m = 0.5) between a pair of demes before onset of reproductive isolation. Although panmixia is a suitable starting point in models of speciation, it is not a useful definition of sympatry in natural populations, because it becomes virtually impossible to find or demonstrate sympatry in nature. The newer, non-spatial definition fails to address the classical debate about whether natural selection within a geographic overlap regularly causes speciation in nature, or whether complete geographic isolation is usually required, We therefore propose a more precise spatial definition by incorporating the population genetics of dispersal (or 'cruising range'). Sympatric speciation is considerably more likely under this spatial definition than under the demic definition, because distance itself has a powerful structuring effect, even over small spatial scales comparable to dispersal. Ecological adaptation in two-dimensional space often acts as a 'magic trait' that causes pleiotropic reductions of gene flow. We provide examples from our own research.

Understanding the process of speciation requires elucidating the processes driving and constraining the evolution of reproductive isolation. For example, reproductive isolation can evolve simply as a by-product of populations adapting to different ecological environments. This process of ‘ecological speciation’ predicts greater levels of reproductive isolation between ecologically-divergent pairs of populations than between ecologically-similar pairs of similar age. The evolution of reproductive isolation can also be promoted by selection against hybrids (reinforcement) and can be constrained by the homogenizing effects of gene flow. This the sis examines the role of selection and gene flow in the evolution of reproductive isolation among host-associated populations of Timema cristinae walking-stick insects. Populations living on different host-plant species (Ceanothus versus Adenostoma) exhibit genetically-based, adaptive divergence in a suite of traits, including color, color-pattern, body size, body shape and behavior. Multiple forms of reproductive isolation were greater between populations using different hosts than between similar-aged populations using the same host. This pattern was detected for habitat isolation, immigrant inviability, sexual isolation, and cryptic postmating isolation, indicating that divergent host-plant adaptation promoted the evolution of multiple reproductive barriers. Conversely, gene flow between populations tended to erode divergence, with the exception of sexual isolation where moderate levels of gene flow promoted reinforcement. Molecular and morphological evidence suggest that the host-associated forms of T. cristinae are unlikely to have achieved species status such that the host forms represent either an ongoing speciation event or population divergence that has reached equilibrium. Studies of more divergent taxa in the genus are required to build up a more complete understanding of how the process of speciation unfolds, from beginning to end.

In multicellular organisms, exchange of genetic information occurs mainly among individuals belonging to the same species through sexual reproduction. Lateral gene transfer between distantly related taxa has been demonstrated in some cases, but its frequency and evolutionary importance have been controversial. By comparing genomes of many grasses, we show that large blocks of DNA containing functional genes are laterally passed among distantly related species. Some of these genes are then used by the recipient species, expanding their genetic toolkit. The spread of functional genes across grasses that have developed distinct physiological and ecological adaptations may therefore represent a significant evolutionary driving force in this globally important group of plants.

Simpson’s fossil-record inspired model of ‘adaptive zones’ proposes that evolution is dominated by small fluctuations within adaptive zones, occasionally punctuated by larger shifts between zones. This model can help explain why the process of population divergence often results in weak or moderate reproductive isolation (RI), rather than strong RI and distinct species. Applied to the speciation process, the adaptive zones hypothesis makes two inter-related predictions: (i) large shifts between zones are relatively rare, (ii) when large shifts do occur they generate stronger RI than shifts within zones. Here, we use ecological, phylogenetic and behavioural data to test these predictions in Timema stick insects. We show that host use in Timema is dominated by moderate shifts within the systematic divisions of flowering plants and conifers, with only a few extreme shifts between these divisions. However, when extreme shifts occur, they generate greater RI than do more moderate shifts. Our results support the adaptive zones model, and suggest that the net contribution of ecological shifts to diversification is dependent on both their magnitude and frequency. We discuss the generality of our findings in the light of emerging evidence from diverse taxa that the evolution of RI is not always the only factor determining the origin of species diversity. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

Ever since Charles Darwin and Alfred Wallace (1858) propelled our understanding about the importance of natural selection in the transformation of species, researchers endeavoured to use this intellectual foundation to explain larger patterns of biodiversity. One pattern emerging from the observation of phylogenetic relationships and ecological adaptations of species is the abundance of lineages, which are apparently rapidly diversifying, resulting in ecologically diverse clades of species. Most of the biodiversity we know is made up by such clades, being the result of so-called adaptive radiations. Phenotypic diversification and lineage accumulation in adaptive radiations have received considerable attention and great progress has been made in understanding these aspects. Adaptive radiations can be triggered by an ecological opportunity, i.e. a newly formed or colonized habitat lacking competing species or the formation of a key-innovation, a novel trait that allows for the invasion of a completely novel set of niches. The radiation of East African cichlid fishes, and other groups of fishes, are hypothesized to have been triggered by a key-innovation, namely a reorganisation of the pharyngeal jaw apparatus (Liem 1973). Liem’s hypothesis attributes the evolutionary success of groups with certain pharyngeal jaw modifications to an increased versatility in exploiting resources. Although morphological descriptions of the pharyngeal jaw apparatus for many taxa of fishes abound in the literature, and studies with functional, biomechanical or ecological perspectives are numerous as well, as of yet no concise treatise about the evolutionary implications of the different aspects and characteristics of the pharyngeal jaw has been published. This gap I thrive to close with the first chapter of this thesis. The course of adaptive radiations might be influenced by a phenomenon only little studied in this context so far. Phenotypic plasticity, the ability of a genotype to produce different phenotypes depending on environmental cues, might increase a founding populations chance of persistence. Novel niches might also be invaded more quickly, since the phenotypic shift due to plasticity might place a population in the ‘realm of attraction’ of a peak on the adaptive landscape. If plasticity is only exhibited in some directions in morphospace, but not in others it has the potential of biasing evolutionary trajectories in adaptive radiations. To better understand if phenotypic plasticity in the pharyngeal jaw might have influenced the adaptive radiations of cichlids, I studied the Nicaraguan Midas cichlid in a common garden experiment. My demonstration of plasticity in the cichlids’ pharyngeal jaw, reported in chapter 2, suggests it as a factor to be considered in answering the question of why there are so many cichlid species. The concept of adaptive radiation is intimately related to ecological adaptation by means of natural selection. Thus, one would not be surprised if phenomena indicative of natural selection would be common in adaptive radiations. One of the strongest cases for the action of natural selection, since the birth of the idea, has been made with the argument of convergent evolution. Separation in time or by geography was, however, assumed to be necessary due to competitive exclusion (Osborn 1902). This principle, later formulated by Gause (1934), was questioned to be applicable to some communities of organisms, one of them being the cichlid species flocks of East Africa. Ernst Mayr (1984) asked: “The coexistence of hundreds of closely related species in the same lake poses some fundamental questions concerning competition and resource utilization. To what extent, if any, is the existence of fish flocks in freshwater lakes in conflict with the concept of competitive exclusion?” This question is investigated in chapter 3, which is concerned with convergence within the cichlid radiation in Lake Tanganyika. The revealed abundance of ecomorphological convergence without geographical or chronological separation indeed seems to defy Gause’s principle. Furthermore, it suggests the facility of coexistence of convergent species to be another key factor for the cichlids’ species richness that has been previously overlooked. The large overlap in morpho- and ecospace between subclades of Tanganyikan cichlids is not unique, but emerges as a common feature of adaptive radiations. This is exemplified by the adaptive radiation of Antarctic notothenioid fishes, the topic of chapter 4, comprising several families, which diversified in parallel along the benthic-pelagic axis. Thus, an adaptive radiation of fishes, taking place in a most different setting than the tropical, confined, freshwater environment in which cichlids diversified, nevertheless exhibits intriguing parallels in subclade overlap. Convergence might hence be a feature of radiations in general.