Partial Reproductive Isolation Research Articles

The role of mycorrhizal fungi in driving ecotype formation in mycoheterotrophic plants

In his seminal paper, Göte Turesson proposed the term ecotype as the ‘ecological unit to cover the product arising as a result of the genotypical response of an ecospecies to a particular habitat'. Turesson further outlined that to fully understand the ecology of a species, a knowledge of its most important ecotypes is needed. Whereas Turesson's original idea of an ecotype mainly referred to the response of a species to abiotic conditions, there is mounting evidence that ecotypes can also originate as a response to biotic conditions. Hence, to understand the ecology of a species, one should also understand the distribution and variation in biotic interactions. For plants, one such biotic interaction involves mycorrhizal fungi. Particularly in mycoheterotrophic plants, i.e. plants that rely on mycorrhizal fungi for their carbon supply, adaptation to and specialization on mycorrhizal fungi have the potential to drive ecotype formation and speciation. In this paper, we provide evidence that populations of mycoheterotrophic plants inhabiting contrasting habitats commonly encounter divergent mycorrhizal fungal communities leading to geographic mosaics of mycorrhizal interactions. Adaptation to local fungal communities, in turn, can induce (partial) reproductive isolation and contribute to ecotype and ultimately species formation as a result of decreased fitness of immigrant genotypes (immigrant inviability). In the most extreme case, loss of photosynthesis and mycorrhizal switching have led to reproductive isolation and the development of novel species that have become fully mycoheterotrophic. Such shifts have occurred repeatedly during the evolutionary history of land plants. We conclude that mycorrhizal fungi not only contribute to the early divergence of populations of mycoheterotrophic plants, but also play a crucial role in the further diversification and origination of this unique set of species that rely on mycorrhizal fungi for obtaining carbon and completing their life cycle.

Genomic signatures of ecological divergence between savanna and forest populations of a Neotropical tree.

In eastern Neotropical South America, the Cerrado, a large savanna vegetation, and the Atlantic Forest harbour high biodiversity levels, and their habitats are rather different from each other. The biomes have intrinsic evolutionary relationships, with high lineage exchange that can be attributed, in part, to a large contact zone between them. The genomic study of ecotypes, i.e. populations adapted to divergent habitats, can be a model to study the genomic signatures of ecological divergence. Here, we investigated two ecotypes of the tree Plathymenia reticulata, one from the Cerrado and the other from the Atlantic Forest, which have a hybrid zone in the ecotonal zone of Atlantic Forest-Cerrado. The ecotypes were sampled in the two biomes and their ecotone. The evolutionary history of the divergence of the species was analysed with double-digest restriction site-associated DNA sequencing. The genetic structure and the genotypic composition of the hybrid zone were determined. Genotype-association analyses were performed, and the loci under putative selection and their functions were investigated. High divergence between the two ecotypes was found, and only early-generation hybrids were found in the hybrid zone, suggesting a partial reproductive barrier. Ancient introgression between the Cerrado and Atlantic Forest was not detected. The soil and climate were associated with genetic divergence in Plathymenia ecotypes and outlier loci were found to be associated with the stress response, with stomatal and root development and with reproduction. The high genomic, ecological and morphophysiological divergence between ecotypes, coupled with partial reproductive isolation, indicate that the ecotypes represent two species and should be managed as different evolutionary lineages. We advise that the forest species should be re-evaluated and restated as vulnerable. Our results provide insights into the genomic mechanisms underlying the diversification of species across savanna and forest habitats and the evolutionary forces acting in the species diversification in the Neotropics.

Two complementary genes in a presence-absence variation contribute to indica-japonica reproductive isolation in rice

Understanding the evolutionary forces in speciation is a central goal in evolutionary biology. Asian cultivated rice has two subspecies, indica and japonica, but the underlying mechanism of the partial reproductive isolation between them remains obscure. Here we show a presence-absence variation (PAV) at the Se locus functions as an indica-japonica reproductive barrier by causing hybrid sterility (HS) in indica-japonica crosses. The locus comprises two adjacent genes: ORF3 encodes a sporophytic pollen killer, whereas ORF4 protects pollen in a gametophytic manner. In F1 of indica-japonica crosses, pollen with the japonica haplotype, which lacks the sequence containing the protective ORF4, is aborted due to the pollen-killing effect of ORF3 from indica. Evolutionary analysis suggests ORF3 is a gene associated with the Asian cultivated rice species complex, and the PAV has contributed to the reproductive isolation between the two subspecies of Asian cultivated rice. Our analyses provide perspectives on rice inter-subspecies post-zygotic isolation, and will promote efforts to overcome reproductive barriers in indica-japonica hybrid rice breeding.

Crossing experiments detect partial reproductive isolation among populations of Triatoma longipennis (Hemiptera: Reduviidae: Triatominae).

Chagas disease is an important vector-borne disease endemic in Mexico. Of the 33 triatomine species found in Mexico, Triatoma longipennis (Usinger) is considered among the most important because of its infection indices, capacity for transmitting Trypanosoma cruzi (Chagas), and its distribution areas. Here, we describe the results of a reproductive isolation analysis among 5 populations of T. longipennis collected from representative areas of Mexico. Fertility and segregation of morphological characteristics were examined in two generations of hybrids. The percentage of pairs with (fertile) offspring varied from 30% to 100% in the parental crosses, while these values varied from 0 to 100% in the intersite crosses. Our results indicate partial reproductive isolation among these populations. These findings shed light on the potential presence of a cryptic species complex of T. longipennis in Mexico.

Geographically consistent hybridization dynamics between the Black-crested and Tufted titmouse with evidence of hybrid zone expansion

Abstract We studied hybridization between the Black-crested and Tufted titmouse across two geographically distinct transects that differ in the timing of secondary contact by hundreds to thousands of years. We found that hybridization patterns correspond to localized hybrid swarms and that the titmouse hybrid zone is likely slowly expanding over time, a product of short post-natal dispersal distances coupled with weak or absent selection against admixture. We show the southern part of the hybrid zone located in Texas is four times wider than the northern region of hybridization in Oklahoma, which is likely due to geographic differences in hybrid zone age. Despite differences in width, most individuals in both transects are advanced-generation hybrids and backcrosses, suggesting geographically consistent hybridization dynamics. We documented a strong correlation between genotypes and plumage index, suggesting that hybridization has not yet resulted in the decoupling of plumage and genome-wide ancestry as observed in some other avian hybrid zones. Although our results suggest the ongoing expansion of the hybrid zone, the rate of expansion appears to be slow, on the scale of tens of meters a year, and it will likely take hundreds of thousands to millions of years before homogenization of the parental populations. While we did not find support for partial reproductive isolation in the hybrid zone itself, there is the possibility that ecological or sexual selection limits introgression into allopatric regions. Broadly, the results of our study highlight the value of multiple, geographically distant, transects across a hybrid zone for assessing the evolutionary dynamics of hybridizing lineages.

Sperm competition experiments reveal low prezygotic postmating isolation between parasitic and nonparasitic lamprey ecotypes.

The role of postmating sexual selection as a potential reproductive barrier in speciation is not well understood. Here, we studied the effects of sperm competition and cryptic female choice as putative postmating barriers in two lamprey ecotypes with a partial reproductive isolation. The European river lamprey Lampetra fluviatilis is anadromous and parasitic of other fish species, whereas the brook lamprey Lampetra planeri is freshwater resident and nonparasitic. We measured sperm traits in both ecotypes and designed sperm competition experiments to test the occurrence of cryptic female choice. We also performed sperm competition experiments either at equal semen volume or equal sperm number to investigate the role of sperm velocity on fertilization success. We observed distinct sperm traits between ecotypes with a higher sperm concentration and a lower sperm velocity for L. planeri compared with L. fluviatilis. The outcomes of sperm competition reflected these differences in sperm traits, and there was no evidence for cryptic female choice irrespective of female ecotype. At equal semen volume, L. planeri males had a higher fertilization success than L. fluviatilis and vice versa at equal sperm number. Our results demonstrate that different sperm traits between ecotypes can influence the male reproductive success and thus gene flow between L. planeri and L. fluviatilis. However, postmating prezygotic barriers are absent and thus cannot explain the partial reproductive isolation between ecotypes.

Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816

We detected five divergent COI lineages in Priapulus caudatus Lamarck, 1816: four from the Arctic and one from the Sea of Okhotsk. K2P distances ranged from 6.87% to 14.35% with a mean distance of 10.03%, which typically corresponds to inter-species distances. However, four of five lineages (excluding the Okhotsk one) were found in syntopy, and no morphological differences between potential species were found. Single-gene phylogenies for the mitochondrial 16S, as well as nuclear 28S, 18S, and FoxQ2 markers, had different topologies and were non-congruent with the COI tree. This may point to an incomplete speciation due to a series of long-time geographical isolations during Pleistocene glaciations in different parts of range of P. caudatus. The 28S and 18S sequences fell into two genotypes, one being found mainly in the intertidal, and the other exclusively in the subtidal, which indicates the prevalence of unidirectional migrations from the intertidal into the subtidal. Because Arctic intertidal populations disappear during glaciations and recover in interglacial periods, and due to their partial reproductive isolation from each other, they give rise to new genetic lineages. Subtidal populations are permanent and have less significant isolation boundaries, therefore they accumulate genetic diversity.

Allopatric origin of sympatric whitefish morphs with insights on the genetic basis of their reproductive isolation.

The European whitefish (Coregonus lavaretus) species complex is a classic example of recent adaptive radiation. Here, we examine a whitefish population introduced to northern Finnish Lake Tsahkal in the late 1960s, where three divergent morphs (viz. littoral, pelagic, and profundal feeders) were found 10 generations after. Using demographic modeling based on genomic data, we show that whitefish morphs evolved during a phase of strict isolation, refuting a rapid sympatric divergence scenario. The lake is now an artificial hybrid zone between morphs originated in allopatry. Despite their current syntopy, clear genetic differentiation remains between two of the three morphs. Using admixture mapping, we identify five SNPs associated with gonad weight variation, a proxy for sexual maturity and spawning time. We suggest that ecological adaptations in spawning time evolved in allopatry are currently maintaining partial reproductive isolation in the absence of other barriers to gene flow.

Speciation with gene flow in a narrow endemic West Virginia cave salamander (Gyrinophilus subterraneus)

Due to their limited geographic distributions and specialized ecologies, cave species are often highly endemic and can be especially vulnerable to habitat degradation within and surrounding the cave systems they inhabit. We investigated the evolutionary history of the West Virginia Spring Salamander (Gyrinophilus subterraneus), estimated the population trend from historic and current survey data, and assessed the current potential for water quality threats to the cave habitat. Our genomic data (mtDNA sequence and ddRADseq-derived SNPs) reveal two, distinct evolutionary lineages within General Davis Cave corresponding to G. subterraneus and its widely distributed sister species, Gyrinophilus porphyriticus, that are also differentiable based on morphological traits. Genomic models of evolutionary history strongly support asymmetric and continuous gene flow between the two lineages, and hybrid classification analyses identify only parental and first generation cross (F1) progeny. Collectively, these results point to a rare case of sympatric speciation occurring within the cave, leading to strong support for continuing to recognize G. subterraneus as a distinct and unique species. Due to its specialized habitat requirements, the complete distribution of G. subterraneus is unresolved, but using survey data in its type locality (and currently the only known occupied site), we find that the population within General Davis Cave has possibly declined over the last 45 years. Finally, our measures of cave and surface stream water quality did not reveal evidence of water quality impairment and provide important baselines for future monitoring. In addition, our unexpected finding of a hybrid zone and partial reproductive isolation between G. subterraneus and G. porphyriticus warrants further attention to better understand the evolutionary and conservation implications of occasional hybridization between the species.

EDNA metabarcoding as a means to assess distribution of subterranean fish communities: Iranian blind cave fishes as a case study

AbstractOne of the most important steps in conservation of the subterranean life forms is to decipher their distribution and ecology, which is challenging using traditional approaches. Development of an environmental DNA (eDNA) assay provides an efficient means for discovering and monitoring subterranean life forms. In this study, the distribution of three Iranian blind cave fish species (blind Iran cave barb Garra typhlops, blind Lorestan cave barb Garra lorestanensis, and blind cave loach Eidinemacheilus smithi) was assessed using 12S rRNA eDNA metabarcoding performed using MiFish‐U PCR primers and preliminary species distribution modeling (SDM) using bioclimatic data. The majority of sampling localities with positive detection of cave barb eDNA fall within suitable habitats in the Zagros Mountains of Iran. Our results revealed that Lorestan and Iran cave barbs have differential distribution patterns, with some extent of habitat overlap in the vicinity of the originally discovered cave barb locality. According to the observed distribution patterns, the blind Lorestan cave barb and cave loach are mostly distributed in habitats close to the Sezar River (Dez River drainage, Iran), and the blind Iran cave barb is distributed towards the west and probably in a few springs in the Karkheh River drainage. Our data support the previously proposed distribution pattern for the cave barbs, in which the species show partial niche separation and reproductive isolation, with the Lorestan cave barb being a water flow‐dependent species and the Iran cave barb being a generalist species preferring variable flow rates. We showed eDNA metabarcoding to be a useful approach for ecological surveys of subterranean fish biodiversity with implications for conservation.

A new variety of Phacelia dubia (Hydrophyllaceae) and a summary of variation and biogeography of the P. dubia complex 1

Occurrences of Phacelia dubia in the Piedmont of South Carolina have been taxonomically enigmatic. Prior work had shown that there was partial reproductive isolation when plants from South Carolina were hybridized with any of the other varieties but evidence of morphological differentiation was lacking. In this study, a new morphological analysis showed South Carolina plants differed significantly in corolla lobe size, sepal size, and leaf dissection in comparisons with neighboring varieties, P. dubia var. dubia and P. dubia var. georgiana. A preponderance of evidence showing differentiation from all other varieties supports recognition of a new variety, P. dubia var. rionensis. Field work and an updated analysis of herbarium records showed the new variety is found in nine contiguous counties in the central and northern Piedmont of South Carolina and two counties in the inner Coastal Plain. We posit a hypothesized biogeographic pathway based on migration of a P. dubia ancestor from the Great Plains or Mexico to the Nashville Basin cedar glades, then to South Carolina piedmont granite outcrops, followed by a migration south to Georgia and Alabama piedmont granite outcrops and a separate migration north to rocky woodlands in North Carolina.

Genetic Divergence between Two Sympatric Ecotypes of Phalaenopsis pulcherrima on Hainan Island

Ecotypes are the result of ecological differentiation at the early stages of speciation. Adaptation to soil conditions offers arguably the best examples of local adaptation in plants. Two sympatric ecotypes, with either a red or green abaxial leaf surface, were found without clear geographical isolation in Phalaenopsis pulcherrima, a Southeast Asia endemic and endangered orchid. The soil of the red leaf ecotype has a higher water content and nutrient content than the green ecotype. What is the genetic structure of the two ecotypes? Is there complete or partial reproductive isolation between the two ecotypes? In this work, leaf reflection of the two ecotypes in P. pulcherrima were compared, to illustrate their difference in leaf color. The genetic differentiation between two ecotypes was examined, using ISSR and SRAP markers to determine the genetic structure of the populations. Our results showed that the green ecotype had reflectance spectrum peaks at 530 nm and 620 nm, while in the red ecotype, the peak at 530 nm was absent. A total of 165 ISSR and SRAP loci showed a high level of genetic diversity within the green ecotype, and analyses of the population structure revealed two genetic clusters that corresponded to the red and green ecotypes. The percentage of variation between the two ecotypes (24.55%) was greater than the percentage of variation among the populations (16.54%)—indicating partial reproductive isolation, high genetic differentiation, and that ecological differentiation has been more important than geographical barriers among populations within ecotypes. Most pairwise FST values between the populations within either ecotype on Hainan Island were less than 0.15; however, the FST between both the Thai and Malaysian populations and the Hainan Island population was greater than 0.25, due to South China sea isolation. Ecotypic differentiation is an important part of speciation; therefore, we must take into account the axes along which lineages sort, when formulating protection strategies.

Recursive adaptation in action: allochronic isolation and divergence of host‐associated populations of the apple maggot fly, Rhagoletis pomonella, following its recent introduction to the western USA

AbstractAn outstanding issue in the study of insect host races concerns the idea of ‘recursive adaptive divergence’, whereby adaptation can occur repeatedly across space and/or time, and the most recent adaptive episode is defined by one or more previously similar cases. The host plant shift of the apple maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae, Carpomyini), from ancestral downy hawthorn [Crataegus mollis (Torr. & A. Gray) Scheele] to introduced, domesticated apple (Malus domestica Borkh.) in the eastern USA has long served as a model system for investigating ecologically driven host race formation in phytophagous insect specialists. Here, we report results from an annual geography survey of eclosion time demonstrating a similar ecological pattern among nascent host‐associated populations of the fly recently introduced ca. 40 years ago from its native range in the east into the Pacific Northwest (PNW) region of the USA. Specifically, using data collected from 25 locations across 5 years, we show that apple‐infesting fly populations in the PNW have rapidly and repeatedly shifted (and maintained differences in) their adult eclosion life‐history timing to infest two novel hawthorn hosts with different fruiting phenologies – a native species (Crataegus douglasii Lindl.) and an introduced species (Crataegus monogyna Jacq.) – generating partial allochronic reproductive isolation in the process. The shifts in the PNW parallel the classic case of host race formation in the eastern USA, but have occurred bi‐directionally to two hawthorn species with phenologies slightly earlier (black hawthorn) and significantly later (ornamental hawthorn) than apple. Our results imply that R. pomonella can both possess and retain extensive‐standing variation (i.e., ‘adaptive memory’) in diapause traits, even following introductions, to rapidly and temporally track novel phenological host opportunities when they arise. Thus, ‘specialized’ host races may not constitute evolutionary dead ends. Rather, adaptive phenotypic and genetic memory may carry over from one host shift to the next, recursively facilitating host race formation in phytophagous insects.

Topography shapes the local coexistence of tree species within species complexes of Neotropical forests.

Forest inventories in Amazonia include around 5000 described tree species belonging to more than 800 genera. Numerous species-rich genera share genetic variation among species because of recent speciation and/or recurrent hybridisation, forming species complexes. Despite the key role that tree species complexes play in understanding Neotropical diversification, and their need to exploit a diversity of niches, little is known about the mechanisms that allow local coexistence of tree species complexes and their species in sympatry. In this study, we explored the fine-scale distribution of five tree species complexes and 22 species within these complexes. Combining forest inventories, botanical determination, and LiDAR-derived topographic data over 120ha of permanent plots in French Guiana, we used a Bayesian modelling framework to test the role of fine-scale topographic wetness and tree neighbourhood on the occurrence of species complexes and the relative distribution of species within complexes. Species complexes of Neotropical trees were widely spread across the topographic wetness gradient at the local scale. Species within complexes showed pervasive niche differentiation along with topographic wetness and competition gradients. Similar patterns of species-specific habitat preferences were observed within several species complexes: species more tolerant to competition for resources grow in drier and less fertile plateaus and slopes. If supported by partial reproductive isolation of species and adaptive introgression at the species complex level, our results suggest that both species-specific habitat specialisation within species complexes and the broad ecological distribution of species complexes might explain the success of these species complexes at the regional scale.

Distinct Adult Eclosion Traits of Sibling Species Rhagoletis pomonella and Rhagoletis zephyria (Diptera: Tephritidae) Under Laboratory Conditions.

Closely related phytophagous insects that specialize on different host plants may have divergent responses to environmental factors. Rhagoletis pomonella (Walsh) and Rhagoletis zephyria Snow (Diptera: Tephritidae) are sibling, sympatric fly species found in western North America that attack and mate on plants of Rosaceae (~60 taxa) and Caprifoliaceae (three taxa), respectively, likely contributing to partial reproductive isolation. Rhagoletis zephyria evolved from R. pomonella and is native to western North America, whereas R. pomonella was introduced there. Given that key features of the flies' ecology, breeding compatibility, and evolution differ, we predicted that adult eclosion patterns of the two flies from Washington State, USA are also distinct. When puparia were chilled, eclosion of apple- and black hawthorn-origin R. pomonella was significantly more dispersed, with less pronounced peaks, than of snowberry-origin R. zephyria within sympatric and nonsympatric site comparisons. Percentages of chilled puparia that produced adults were ≥67% for both species. However, when puparia were not chilled, from 13.5 to 21.9% of apple-origin R. pomonella versus only 1.2% to 1.9% of R. zephyria eclosed. The distinct differences in eclosion traits of R. pomonella and R. zephyria could be due to greater genetic variation in R. pomonella, associated with its use of a wider range of host plants than R. zephyria.

Defining and Disrupting Species Boundaries in Saccharomyces.

The genus Saccharomyces is an evolutionary paradox. On the one hand, it is composed of at least eight clearly phylogenetically delineated species; these species are reproductively isolated from each other, and hybrids usually cannot complete their sexual life cycles. On the other hand, Saccharomyces species have a long evolutionary history of hybridization, which has phenotypic consequences for adaptation and domestication. A variety of cellular, ecological, and evolutionary mechanisms are responsible for this partial reproductive isolation among Saccharomyces species. These mechanisms have caused the evolution of diverse Saccharomyces species and hybrids, which occupy a variety of wild and domesticated habitats. In this article, we introduce readers to the mechanisms isolating Saccharomyces species, the circumstances in which reproductive isolation mechanisms are effective and ineffective, and the evolutionary consequences of partial reproductive isolation. We discuss both the evolutionary history of the genus Saccharomyces and the human history of taxonomists and biologists struggling with species concepts in this fascinating genus.

The impact of global selection on local adaptation and reproductive isolation.

Despite the homogenizing effect of strong gene flow between two populations, adaptation under symmetric divergent selection pressures results in partial reproductive isolation: adaptive substitutions act as local barriers to gene flow, and if divergent selection continues unimpeded, this will result in complete reproductive isolation of the two populations, i.e. speciation. However, a key issue in framing the process of speciation as a tension between local adaptation and the homogenizing force of gene flow is that the mutation process is blind to changes in the environment and therefore tends to limit adaptation. Here we investigate how globally beneficial mutations (GBMs) affect divergent local adaptation and reproductive isolation. When phenotypic divergence is finite, we show that the presence of GBMs limits local adaptation, generating a persistent genetic load at the loci that contribute to the trait under divergent selection and reducing genome-wide divergence. Furthermore, we show that while GBMs cannot prohibit the process of continuous differentiation, they induce a substantial delay in the genome-wide shutdown of gene flow.This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers’.

Pelagic-benthic resource polymorphism in Schizopygopsis thermalis Herzenstein 1891 (Pisces, Cyprinidae) in a headwater lake in the Salween River system on the Tibetan Plateau.

Resource polymorphism is a ubiquitous phenomenon in vertebrates and may represent a critical intermediate stage in speciation. Freshwater lakes in high‐altitude areas represent a natural system for understanding resource polymorphism in fishes benefiting from diverse lacustrine environments and species‐poor fish assemblages. We report resource polymorphism in a cyprinid fish, Schizopygopsis thermalis, in Lake Amdo Tsonak Co, a headwater lake in the upper Salween River system. Two discrete intraspecific morphs, planktivorous and benthivorous, were identified according to geometric morphometrics and traditional univariate linear measures. The planktivorous morph exhibits a longer head, longer upper and lower jaw, larger asymptotic standard length (L∞), lower growth rate (k), and higher growth performance index (φ) than the benthivorous morph. With respect to descriptive traits, the planktivorous morph possesses a large, terminal mouth and obvious mucus pores on the cheek and chin, while the benthivorous morph is characterized by a more inferior mouth with a sharpen horny edge on the lower jaw and unconspicuous mucus pores. The discrete pelagic–benthic resources and low interspecific competition in the lake system might drive the initial differentiation of the two morphs, and partial spatial reproductive isolation in breeding further maintains and reinforces the differences between them.

Hybrid zone genomics supports candidate species in Iberian Alytes obstetricans

Abstract While estimates of genetic divergence are increasingly used in molecular taxonomy, hybrid zone analyses can provide decisive evidence for evaluating candidate species. Applying a population genomic approach (RAD-sequencing) to a fine-scale transect sampling, we analyzed the transition between two Iberian subspecies of the common midwife toad (Alytes obstetricans almogavarii and A. o. pertinax) in Catalonia (northeastern Spain), which putatively diverged since the Plio-Pleistocene. Their hybrid zone was remarkably narrow, with extensive admixture restricted to a single locality (close to Tarragona), and congruent allele frequency clines for the mitochondrial (13 km wide) and the average nuclear genomes (16 km wide). We also fitted clines independently for 89 taxon-diagnostic SNPs: most of them behave like the nuclear background, but a subset (13%) is completely impermeable to gene flow and might be linked to barrier loci involved in hybrid incompatibilities. Assuming that midwife toads are able to disperse in the area of contact, we conclude that these taxa experience partial reproductive isolation and represent incipient species, i.e. Alytes almogavarii and Alytes obstetricans. Interestingly, their evolutionary age and mitochondrial divergence fall below the thresholds proposed in molecular systematics studies, emphasizing the difficulty of predicting the outcome of secondary contacts between young lineages entering the grey zone of speciation.

Ecological speciation in European whitefish is driven by a large-gaped predator.

Lake‐dwelling fish that form species pairs/flocks characterized by body size divergence are important model systems for speciation research. Although several sources of divergent selection have been identified in these systems, their importance for driving the speciation process remains elusive. A major problem is that in retrospect, we cannot distinguish selection pressures that initiated divergence from those acting later in the process. To address this issue, we studied the initial stages of speciation in European whitefish (Coregonus lavaretus) using data from 358 populations of varying age (26–10,000 years). We find that whitefish speciation is driven by a large‐growing predator, the northern pike (Esox lucius). Pike initiates divergence by causing a largely plastic differentiation into benthic giants and pelagic dwarfs: ecotypes that will subsequently develop partial reproductive isolation and heritable differences in gill raker number. Using an eco‐evolutionary model, we demonstrate how pike's habitat specificity and large gape size are critical for imposing a between‐habitat trade‐off, causing prey to mature in a safer place or at a safer size. Thereby, we propose a novel mechanism for how predators may cause dwarf/giant speciation in lake‐dwelling fish species.