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For polyploid species to persist, they must be reproductively isolated from their diploid parental species, which coexist at the same time and place at least initially. In a complex of biparentally reproducing tetraploid and diploid tree frogs in North America, selective phonotaxis—mediated by differences in the pulse-repetition (pulse rate) of their mate-attracting vocalizations—ensures assortative mating. We show that artificially produced autotriploid females of the diploid species (Hyla chrysoscelis) show a shift in pulse-rate preference in the direction of the pulse rate produced by males of the tetraploid species (Hyla versicolor). The estimated preference function is centred near the mean pulse rate of the calls of artificially produced male autotriploids. Such a parallel shift, which is caused by polyploidy per se and whose magnitude is expected to be greater in autotetraploids, may have facilitated sympatric speciation by promoting reproductive isolation of the initially formed polyploids from their diploid parental forms. This process also helps to explain why tetraploid lineages with different origins have similar advertisement calls and freely interbreed.

The notion that shifts to new hosts can initiate insect speciation is more than 150 years old, yet widespread conflation with paradigms of sympatric speciation has led to confusion about how much support exists for this hypothesis. Here, we review 85 insect systems and evaluate the relationship between host shifting, reproductive isolation, and speciation. We sort insects into five categories: (1) systems in which a host shift has initiated speciation; (2) systems in which a host shift has made a contribution to speciation; (3) systems in which a host shift has caused the evolution of new reproductive isolating barriers; (4) systems with hostassociated genetic differences; and (5) systems with no evidence of host-associated genetic differences. We find host-associated genetic structure in 65 systems, 43 of which show that host shifts have resulted in the evolution of new reproductive barriers. Twenty-six of the latter also support a role for host shifts in speciation, including eight studies that definitively support the hypothesis that a host shift has initiated speciation. While this review is agnostic as to the fraction of all insect speciation events to which host shifts have contributed, it clarifies that host shifts absolutely can and do initiate speciation.

Assortative mating occurs when there is a correlation (positive or negative) between male and female phenotypes or genotypes across mated pairs. To determine the typical strength and direction of assortative mating in animals, we carried out a meta-analysis of published measures of assortative mating for a variety of phenotypic and genotypic traits in a diverse set of animal taxa. We focused on the strength of assortment within populations, excluding reproductively isolated populations and species. We collected 1,116 published correlations between mated pairs from 254 species (360 unique species-trait combinations) in five phyla. The mean correlation between mates was 0.28, showing an overall tendency toward positive assortative mating within populations. Although 19% of the correlations were negative, simulations suggest that these could represent type I error and that negative assortative mating may be rare. We also find significant differences in the strength of assortment among major taxonomic groups and among trait categories. We discuss various possible reasons for the evolution of assortative mating and its implications for speciation.

The extraordinary species richness of freshwater fishes has attracted much research on mechanisms and modes of speciation. We here review research on speciation in freshwater fishes in light of speciation theory, and place this in a context of broad-scale diversity patterns in freshwater fishes. We discuss several major repeated themes in freshwater fish speciation and the speciation mechanisms they are frequently associated with. These include transitions between marine and freshwater habitats, transitions between discrete freshwater habitats, and ecological transitions within habitats, as well as speciation without distinct niche shifts. Major research directions in the years to come include understanding the transition from extrinsic environment-dependent to intrinsic reproductive isolation and its influences on species persistence and understanding the extrinsic and intrinsic constraints to speciation and how these relate to broad-scale diversification patterns through time.

Inferring the geographic mode of speciation could help reveal the evolutionary and ecological mechanisms that underlie the generation of biodiversity. Comparative methods have sought to reconstruct the geographic speciation history of clades, using data on phylogeny and species geographic ranges. However, inference from comparative methods has been limited by uncertainty over whether contemporary biodiversity data retain the historic signal of speciation. We constructed a process-based simulation model to determine the influence of speciation mode and postspeciation range evolution on current biodiversity patterns. The simulations suggest that the signal of speciation history remains detectable in species distributions and phylogeny, even when species ranges have evolved substantially through time. We extracted this signal by using acombination of summary statistics that had good power to distinguish speciation modes and then used these statistics to infer the speciation history of 30 plant and animal clades. The results point to broad taxonomic patterns in the modes of speciation, with strongest support for founder speciation in mammals and birds and strongest support for sympatric speciation in plants. Our model and analyses show that broad-scale comparative methods can be a powerful complementary approach to more focused genomic analyses in the study of the patterns and mechanisms of speciation.

In plants, the mechanism for ecological sympatric speciation (SS) is little known. Here, after ruling out the possibility of secondary contact, we show that wild emmer wheat, at the microclimatically divergent microsite of “Evolution Canyon” (EC), Mt. Carmel, Israel, underwent triple SS. Initially, it split following a bottleneck of an ancestral population, and further diversified to three isolated populations driven by disruptive ecological selection. Remarkably, two postzygotically isolated populations (SFS1 and SFS2) sympatrically branched within an area less than 30 m at the tropical hot and dry savannoid south-facing slope (SFS). A series of homozygous chromosomal rearrangements in the SFS1 population caused hybrid sterility with the SFS2 population. We demonstrate that these two populations developed divergent adaptive mechanisms against severe abiotic stresses on the tropical SFS. The SFS2 population evolved very early flowering, while the SFS1 population alternatively evolved a direct tolerance to irradiance by improved ROS scavenging activity that potentially accounts for its evolutionary fate with unstable chromosome status. Moreover, a third prezygotically isolated sympatric population adapted on the abutting temperate, humid, cool, and forested north-facing slope (NFS), separated by 250 m from the SFS wild emmer wheat populations. The NFS population evolved multiple resistant loci to fungal diseases, including powdery mildew and stripe rust. Our study illustrates how plants sympatrically adapt and speciate under disruptive ecological selection of abiotic and biotic stresses.

In allopatric populations, geographical separation simultaneously isolates the entire genome, allowing genetic divergence to accumulate virtually anywhere in the genome. In sympatric populations, however, the strong divergent selection required to overcome migration produces a genetic mosaic of divergent and non-divergent genomic regions. In some recent genome scans, each divergent genomic region has been interpreted as an independent incidence of migration/selection balance, such that the reduction of gene exchange is restricted to a few kilobases around each divergently selected gene. I propose an alternative mechanism, ‘divergence hitchhiking’ (DH), in which divergent selection can reduce gene exchange for several megabases around a gene under strong divergent selection. Not all genes/markers within a DH region are divergently selected, yet the entire region is protected to some degree from gene exchange, permitting genetic divergence from mechanisms other than divergent selection to accumulate secondarily. After contrasting DH and multilocus migration/selection balance (MM/SB), I outline a model in which genomic isolation at a given genomic location is jointly determined by DH and genome-wide effects of the progressive reduction in realized migration, then illustrate DH using data from several pairs of incipient species in the wild.

Vascular epiphytes are an important component of many ecosystems and constitute a substantial part of global plant diversity. In this context, accidental epiphytism, that is, the opportunistic epiphytic growth of typically terrestrial species, deserves special attention because it provides crucial insights into the global distribution of vascular epiphytes and the initial evolution of epiphytic lineages. Even though accidental epiphytes have been mentioned in the literature for more than a century, they have been neglected in most epiphyte studies. Only recently has accidental epiphytism been investigated more thoroughly. Therefore, the aim of this article is to provide a comprehensive review of the ecological basis and evolutionary relevance of this common but largely neglected phenomenon and to highlight open questions and promising research directions. Our central statement—that any species has the potential to grow epiphytically given the availability of suitable microhabitats and successful dispersal—is backed up by a compilation of observations of accidental epiphytes from numerous ecosystems with diverse climates, even including semiarid Mediterranean ones. A variety of arboreal microhabitats and environmental conditions conform to the ecological niche of typical terrestrial species, with the availability of such microhabitats depending on the interaction of local climate conditions, host tree age, and host species identity. Whenever suitable microhabitats are available in tree crowns, accidental epiphytism is limited primarily by dispersal. In an evolutionary context, the conquest of forest canopy represents an ecological opportunity where accidental epiphytes act as links between terrestrial and epiphytic life forms. We discuss two fundamental scenarios with sympatric speciation, selective pressure, autopolyploidy, and allopatric speciation as underlying mechanisms in the transition from terrestrial to epiphytic growth. In conclusion, we argue that accidental epiphytism is a substrate and dispersal-dependent phenomenon and that, both from an individual perspective and an evolutionary perspective, epiphytism reflects the occupation of suitable but previously unexploited arboreal microhabitats. Acknowledging the fundamental principles that plant growth is opportunistic and that dispersal is a stochastic process can decisively improve our understanding of species distributions and other ecological patterns, as in the case of accidental epiphytism.

Understanding the processes underlying the origin of species is a fundamental goal of biology. It is widely accepted that speciation requires an interruption of gene flow between populations: ongoing gene exchange is considered a major hindrance to population divergence and, ultimately, to the evolution of new species. Where a geographic barrier to reproductive isolation is lacking, a biological mechanism for speciation is required to counterbalance the homogenizing effect of gene flow. Speciation with initially strong gene flow is thought to be extremely rare, and few convincing empirical examples have been published. However, using phylogenetic, karyological, and ecological data for the flora of a minute oceanic island (Lord Howe Island, LHI), we demonstrate that speciation with gene flow may, in fact, be frequent in some instances and could account for one in five of the endemic plant species of LHI. We present 11 potential instances of species divergence with gene flow, including an in situ radiation of five species of Coprosma (Rubiaceae, the coffee family). These results, together with the speciation of Howea palms on LHI, challenge current views on the origin of species diversity.

Speciation with ongoing homogenizing gene flow, later dubbed sympatric speciation, has been a fascinating and debated topic since Darwin proposed it. Here, we analyzed sympatric speciation of the spiny mouse, Acomys cahirinus, from Evolution Canyon I, Mount Carmel, Israel, revealed by whole-genome, methylome, and behavior comparisons. Mitochondrial phylogeny indicated that the tropical African Slope (AS) and temperate European Slope (ES) populations were sister taxa and shared a common ancestor. Based on the de novo chromosomal-level genome, we compared the genome and methylome of the two populations from EC I. We found clear-cut divergences between them based on both single nucleotide polymorphisms (SNPs) and structure variations (SVs). We identified 440 highly diverged regions and found olfactory receptors significantly divergent between slopes, suggesting prezygotic reproductive isolation. Furthermore, genes related to adaptation were enriched in immunity, temperature homeostasis in AS and energy, and cell cycle in ES. Population demographic modeling showed that the AS and ES populations split from the same ancestor with decreasing gene flow, implying sympatric speciation. Epigenetic methylation divergence preceded genetic differentiation and facilitated slope adaptation and sympatric speciation. We found a significant difference in activity onset in laboratory between the two populations, associated with the methylation divergence of circadian genes. We concluded that behavioral, genomic, and methylomic divergence substantiated sympatric speciation of Acomys from EC I in Israel, shown earlier transcriptomically.