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Illustration of the proposed evolutionary scenario of hybrid parallel speciation and a comparison to classical hybrid speciation. A scenario consistent with our results is one of initial speciation from a blue ancestor into P. pundamilia and P. nyererei (here represented by the populations at Makobe Island, M), followed much later by the colonization of the Mwanza Gulf (including Python Island, P) by P. pundamilia. Later again P. nyererei arrive in the Mwanza Gulf, hybridize with the local P. pundamilia population and merge into a hybrid population that carries a mixture of genetic variation from both species. This hybrid population speciates again into sympatric P. sp. 'pundamilia-like' and P. sp. 'nyererei-like'. There is strong assortative mating between P. sp. 'pundamilia-like' and P. sp. 'nyererei-like' at Python (illustrated by the crossed green lines, Selz, et al. 2014b) and also some evidence for assortative mating between individuals of P. sp. 'nyererei-like' from Python and individuals of the original P. nyererei from Makobe Island (Selz et al. 2016). 'Hybrid parallel speciation' relies on the local availability of the ecological niches of both the local and the geographically distant parental species giving hybrids with alternative trait combinations fitness advantages in different parts of the ecological range of the hybrid population. Should the geographical ranges of P. sp. 'nyererei-like' and P. nyererei ever expand sufficiently to meet, the ecological and phenotypic similarity of these species may predict that the species merge into a single species. In contrast, classical hybrid speciation (right panel) produces one species of hybrid origin that may be ecologically distinct and reproductively isolated from both parental species and can hence coexist in sympatry with both. We exemplify hybrid speciation in Lake Victoria cichlids with Mbipia mbipi which may have resulted from hybridization between M. lutea and P. pundamilia (Keller et al. 2013). Larger evolutionary distance between the parental species (illustrated by multiple intermittent speciation events) may facilitate the formation of a hybrid species as more incompatibilities are expected to segregate in the hybrid population, and the novel ecological and/or sexual trait combinations may be more transgressive and differ from both parental species along more phenotypic axes of divergence (Selz et al. 2014a,c). Hybrid speciation requires either an underutilized niche that the hybrid species can exploit better than either parental species or geographical distance to the parental species. In the case of 'hybrid parallel speciation', on the other hand, two species are generated from a hybrid population that are reproductively isolated and ecologically distinct from each other but that are expected to be ecologically and phenotypically similar to the two parental species. Hybrid speciation and 'hybrid parallel speciation' represent different outcomes of a continuum of possible ways by which admixture variation may be involved in speciation, varying in extent of ecological differentiation and reproductive isolation within the hybrid population and between the hybrid population and its parental species, mediated by the geographical context, niche availability and the genetic similarity between the parental species.
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Modes and mechanisms of speciation are best studied in young species pairs. In older taxa it is increasingly difficult to distinguish what happened during speciation from what happened after speciation. Lake Victoria cichlids in the genus Pundamilia encompass a complex of young species and polymorphic populations. One Pundamilia species pair, P. pu...
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Citations
... Sample IDs, source (newly sampled, previous studies or MNCN), sampling permits and GPS coordinates are in Table S1. study also had a restricted sampling of the putative parental species, especially of S. 132 carolitertii, since only one population from the Mondego River Basin was available, which 133 is at the southern edge of the S. carolitertii distribution and the northern edge of the S. for example, to investigate the role of gene flow in the ecological speciation of 167 sticklebacks (Marques et al., 2019) and in the parallel origin of cichlids species pairs 168 (Meier, Sousa, et al., 2017), as well as introgression with a now extinct ghost lineage in 169 the intertidal goby Chaenogobius annularis (Kato et al., 2024). These methods have also 170 been previously employed to investigate the divergence process in the Iberian chubs 171 system, albeit with limited success due to the limited number of genetic markers (Mendes 172 et al., 2021). ...
Hybridization - the successful reproductive cross between individuals from different species - is increasingly recognized as a relatively common phenomenon in nature, mostly due to the increasing availability of genomic data for many organisms and the development of sophisticated methods to detect past gene flow. As a result, evidence of past gene flow has been detected in the genomes of many species, allowing us to investigate the evolutionary forces that act upon hybrid genomes. Biological systems where multiple instances of hybridization have been detected at different time scales are especially useful for this, as they allow investigating the effects of selection and recombination at different time scales post-hybridization. The Iberian chubs ( Squalius spp. ) present an ideal study system for this. In this group of primary fish inhabiting the rivers of the Iberian Peninsula, multiple instances of past hybridization at different geographical and time scales were reported between different species. However, before we investigate the effects of selection and recombination, it is crucial that we date the hybridization events and quantify the contribution from each parental species. In this study, we infer the demographic history of two Iberian chub hybrid lineages, one resulting from a proposed ancient hybridization event ( S. pyrenaicus ) and another potentially much more recent (São Martinho). We generated whole genome resequencing data for 52 individuals from the two hybrid lineages and their putative parental populations. Our demographic modelling results confirm the hypothesis of ancient hybridization between S. carolitertii and S. tartessicus around 600,000-800,000 years ago, giving rise to the S. pyrenaicus lineage. We also confirm that S. carolitertii is the major parental, with S. tartessicus only contributing <10% to the S. pyrenaicus genome. Furthermore, we confirm the more recent hybridization between S. caetobrigu s and S. pyrenaicus (around 4500 years ago) in the São Martinho population. We observe similar contributions from both parental species (around 50%) to the genome of the individuals of this population. Overall, our results give us a deeper understanding of how and when these past gene flow events happened and the contributions of each parental species to the genomes of the individuals of the hybrid lineages.
... We narrowed down to 28 chromosomes per population, that is, 14 diploid individuals, to project the SFS. We tested five models (see Figure 5): 'no gene flow', 'constant gene flow', 'ancient gene flow', 'recent gene flow' and 'different gene flow' by following Meier et al. (2017). For these five models, we drew priors from a log uniform distribution. ...
In the marine realm, unidirectional ocean currents often lead to high migration rates of marine organisms and, therefore, inhibit the formation of their latitudinal genetic structure. In contrast, cryptic latitudinal structures associated with local adaptation may frequently exist in widespread species generally exposed to a strong environmental heterogeneity. However, our understanding of the evolvability of locally adapted populations in open marine environments still needs to be completed. The coastal area along the Sea of Japan, where the Tsushima Warm Current flows from south to north in the Japanese Archipelago, provides a good model system for exploring this question. This study explored evidence for latitudinal local adaptation along with the prevailing ocean current in the ice goby Leucopsarion petersii at the phenotypic and genomic levels. Common garden experiments clearly showed genetically based clinal variation in growth rate, strongly suggesting local adaptation through conutergradient selection of this fitness‐related trait. Analyses based on reduced‐representation sequencing revealed a slight signal of genetic differentiation between the southern and northern populations, although continuous historical gene flow between them was supported by demographic modelling. Also, whole‐genome resequencing showed their independent demographic history during the last glacial period. Thus, these results suggest that gene flow along with the prevailing ocean current is somewhat limited, and the populations are not completely panmictic. Furthermore, the selection scan based on low‐coverage genome‐wide sequencing detected putative genomic signatures of latitudinal adaptation of growth‐related genes. Thus, our integrative study provided a novel example of marine local adaptation under a large ocean current.
... The threshold for observed SFS entry count set as 10 (-C 10). Following the method in Meier et al. [72], the likelihood estimation for each model was repeated 100 times using the parameter values estimated in the run with the highest log-likelihood to compute the AIC distribution. The AIC distributions were compared across the models to estimate the best model. ...
Background
Floodplains harbor highly biodiverse ecosystems, which have been strongly affected by both past climate change and by recent human activities, resulting in a high prevalence of many endangered species in these habitats. Understanding the history of floodplain species over a wide range of timescales can contribute to effective conservation planning. We reconstructed the population formation history of the Itasenpara bitterling Acheilognathus longipinnis, an endangered floodplain fish species in Japan, over a broad timescale based on phylogenetic analysis, demographic modeling, and historical demographic analysis using mitogenome and whole-genome sequences. A genome sequence was newly assembled as a reference for the resequencing analysis. This bitterling is distributed in three plains separated by high mountain ranges and exhibits ecological characteristics well adapted to floodplain environments.
Results
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Conclusions
Our results suggest that the floodplain bitterling was able to disperse through unknown routes after mountain uplift and that its populations were strongly influenced by climatic and geographic changes in glacial–interglacial cycles and subsequent human activities, probably related to its floodplain-dependent ecology. The genomic data highlight the unanticipated distribution process of this species and the magnitude of the impact of human activities, with important implications for its conservation.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12862-024-02326-y.
... The isolation-by-distance (IBD) analysis for the Pundamilia and Neochromis species complexes excluded locations in the upstream part of the Mwanza gulf due to local environmental factors. Specifically, turbidity-driven adaptation in head morphology and hybridization between P. pundamilia and P. nyererei in the southern part of the gulf (Seehausen, 1996;Magalhaes et al., 2009;Meier et al., 2017) likely disrupted the expected ring-like distribution pattern. ...
... In most cases of ring speciation, progressive divergence of intermediate forms along the barrier can be attributed to ecological, behavioural, or geographical processes (Irwin et al., 2001 b). One of the major drivers of speciation in Lake Victoria cichlids is assortative mating based on male nuptial coloration, which rapidly raises reproductive isolation between colour morphs even in closely related species (Seehausen, 1997;Magalhaes et al., 2010;Meier et al., 2017). While high colour polymorphism seems to be selected for in cichlids, many correlations between coloration and environmental parameters such as turbidity or habitat type (rocks, open water, vegetation) suggest that male visual attributes, thus speciation, could be constrained by the environment (Seehausen et al., 1999;Seehausen et al., 2008) even in the closely related species of the Pundamilia genus (Carleton et al., 2005). ...
Ring species provide a valuable framework for studying intermediate steps of speciation resulting in two new species. Classic examples of ring species have involved large spatial and temporal scales-and this is partly why few idealised cases exist. In contrast, we focus on two species complexes of cichlid fishes from Southern Lake Victoria that evolved rapidly within the last 15,000 years across relatively small geographic space. We reconstruct the path to speciation between two forms of Pundamilia and Neochromis species that exist in a ring-like distribution around deep water, which acts as a dispersal barrier for these shallow water adapted fishes. We test key predictions of ring-like biogeography, population connectivity, terminal overlap and differentiation in mating and ecological traits. Our results indicate that both species complexes show a gradual change in craniofacial morphology along a ring-like distribution, corresponding to diet shifts. This phenotypic change is correlated with geographical distance in both rings, although they appear to have spatially different evolutionary trajectories. Sympatric species at the ends of both rings exhibit signs of convergent and divergent ecological character displacement in several craniofacial traits, potentially explaining their coexistence. In contrast to craniofacial morphology, male nuptial colouration changes abruptly in both rings, with the change occurring at the end of the ring in Pundamilia and early in Neochromis. We discuss the influence of environmental factors on the observed phenotypic variation and how resistance to connectivity might alter the isolation-by-distance pattern. Our study provides compelling evidence of how concerted changes in mating and ecological traits during isolation by distance can lead to new species and highlights the importance of parapatric speciation in adaptive radiation.
... In a third step, the best-supported scenario including all diploids was used as backbone to infer the origin of the tetraploids by individually branching each of the six tetraploid geographical groups in all possible topologies consistent either with an origin from a single diploid population without concomitant or secondary gene flow or an origin involving a basal or secondary admixture event as was for instance shown in diploidautotetraploid Arabidopsis arenosa (Arnold et al., 2015) ( Fig. S3c). Finally, demographic parameters of the best-fitting scenario were estimated for each tetraploid geographical group by running coalescent models with 50 bootstrapped dataset replicates (Meier et al., 2017;Marques et al., 2019) performing 25 independent runs for each dataset. ...
Early studies of the textbook mixed‐ploidy system Biscutella laevigata highlighted diploids restricted to never‐glaciated lowlands and tetraploids at high elevations across the European Alps, promoting the hypothesis that whole‐genome duplication (WGD) is advantageous under environmental changes. Here we addressed long‐held hypotheses on the role of hybridisation at the origin of the tetraploids, their single vs multiple origins, and whether a shift in climatic niche accompanied WGD.
Climatic niche modelling together with spatial genetics and coalescent modelling based on ddRAD‐seq genotyping of 17 diploid and 19 tetraploid populations was used to revisit the evolution of this species complex in space and time.
Diploids differentiated into four genetic lineages corresponding to allopatric glacial refugia at the onset of the last ice age, whereas tetraploids displaying tetrasomic inheritance formed a uniform group that originated from southern diploids before the last glacial maximum. Derived from diploids occurring at high elevation, autotetraploids likely inherited their adaptation to high elevation rather than having evolved it through or after WGD. They further presented considerable postglacial expansion across the Alps and underwent admixture with diploids.
Although the underpinnings of the successful expansion of autotetraploids remain elusive, differentiation in B. laevigata was chiefly driven by the glacial history of the Alps.
... 'Luanso'). These species pairs of Pundamilia represent replicate speciation events [31]. The sampled cichlid species vary in their micro-habitat and trophic specialisations [2,3,18,51,65] and also in the extent of genetic differentiation [31,32]. ...
... These species pairs of Pundamilia represent replicate speciation events [31]. The sampled cichlid species vary in their micro-habitat and trophic specialisations [2,3,18,51,65] and also in the extent of genetic differentiation [31,32]. Within the radiation, divergence is 14,600 years old, while the divergence between both non-radiating lineages, and between them and the ancestors of the radiations in Lake Victoria, Lake Malawi and other lakes, is 8-10 million years old [31,32,48]. ...
... The sampled cichlid species vary in their micro-habitat and trophic specialisations [2,3,18,51,65] and also in the extent of genetic differentiation [31,32]. Within the radiation, divergence is 14,600 years old, while the divergence between both non-radiating lineages, and between them and the ancestors of the radiations in Lake Victoria, Lake Malawi and other lakes, is 8-10 million years old [31,32,48]. Fish were immediately sacrificed with an overdose of 2phenoxyethanol, numbered and preserved in ethanol (some directly preserved in 100% ethanol, others fixed in 4% formaldehyde and then transferred to 70% ethanol). ...
African cichlids are model systems for evolutionary studies and host-parasite interactions, because of their adaptive radiations and because they harbour many species of monogenean parasites with high host-specificity. Five locations were sampled in southern Lake Victoria: gill-infecting monogeneans were surveyed from 18 cichlid species belonging to this radiation superflock and two others representing two older and distantly related lineages. We found one species of Gyrodactylidae, Gyrodactylus sturmbaueri Vanhove, Snoeks, Volckaert & Huyse, 2011, and seven species of Dactylogyridae. Four are described herein: Cichlidogyrus pseudodossoui n. sp., Cichlidogyrus nyanza n. sp., Cichlidogyrus furu n. sp., and Cichlidogyrus vetusmolendarius n. sp. Another Cichlidogyrus species is reported but not formally described (low number of specimens, morphological similarity with C. furu n. sp.). Two other species are redescribed: C. bifurcatus Paperna, 1960 and C. longipenis Paperna & Thurston, 1969. Our results confirm that the monogenean fauna of Victorian littoral cichlids displays lower species richness and lower host-specificity than that of Lake Tanganyika littoral cichlids. In C. furu n. sp., hooks V are clearly longer than the others, highlighting the need to re-evaluate the current classification system that considers hook pairs III–VII as rather uniform. Some morphological features of C. bifurcatus, C. longipenis, and C. nyanza n. sp. suggest that these are closely related to congeners that infect other haplochromines. Morphological traits indicate that representatives of Cichlidogyrus colonised Lake Victoria haplochromines or their ancestors at least twice, which is in line with the Lake Victoria superflock being colonised by two cichlid tribes (Haplochromini and Oreochromini).
... Nevertheless, the traits that evolved repeatedly in parallel are often assumed to have arisen independently through separate de novo mutations (narrow-sense definition of parallel evolution), but such mutations could also have been recruited from shared ancestral polymorphisms or interspecific gene flow [10][11][12]. For example, widespread parallel evolution in sticklebacks was due to repeated fixation of ectodysplasin alleles [13], and Pundamilia cichlid species appeared after hybridization [14,15]. ...
... Systems with either parallel evolution or parallel maintenance of species differences are thus both useful for studying the processes underlying natural selection in the evolution of species or traits [12,14]. It is crucial to study the underlying evolutionary mechanisms of parallel evolution, including natural selection, de novo mutations, gene flow, drift and standing genetic variation [14,44]. ...
... Systems with either parallel evolution or parallel maintenance of species differences are thus both useful for studying the processes underlying natural selection in the evolution of species or traits [12,14]. It is crucial to study the underlying evolutionary mechanisms of parallel evolution, including natural selection, de novo mutations, gene flow, drift and standing genetic variation [14,44]. However, tests discriminating single and multiple origins [45] found that A. ecalcarata is not monophyletic. ...
Background
The parallel evolution of similar traits or species provides strong evidence for the role of natural selection in evolution. Traits or species that evolved repeatedly can be driven by separate de novo mutations or interspecific gene flow. Although parallel evolution has been reported in many studies, documented cases of parallel evolution caused by gene flow are scarce by comparison. Aquilegia ecalcarata and A. kansuensis belong to the genus of Aquilegia , and are the closest related sister species. Mutiple origins of A. ecalcarata have been reported in previous studies, but whether they have been driven by separate de novo mutations or gene flow remains unclear.
Results
In this study, We conducted genomic analysis from 158 individuals of two repeatedly evolving pairs of A. ecalcarata and A. kansuensis . All samples were divided into two distinct clades with obvious geographical distribution based on phylogeny and population structure. Demographic modeling revealed that the origin of the A. ecalcarata in the Eastern of China was caused by gene flow, and the Eastern A. ecalcarata occurred following introgression from Western A. ecalcarata population. Analysis of Treemix and D -statistic also revealed that a strong signal of gene flow was detected from Western A. ecalcarata to Eastern A. ecalcarata. Genetic divergence and selective sweep analyses inferred parallel regions of genomic divergence and identified many candidate genes associated with ecologically adaptive divergence between species pair. Comparative analysis of parallel diverged regions and gene introgression confirms that gene flow contributed to the parallel evolution of A. ecalcarata .
Conclusions
Our results further confirmed the multiple origins of A. ecalcarata and highlighted the roles of gene flow. These findings provide new evidence for parallel origin after hybridization as well as insights into the ecological adaptation mechanisms underlying the parallel origins of species.
... We observed the lowest cross-validation error rate for K = 2 (Fig. S1b), reflecting the young age 9 of radiation and ongoing introgressions of Lake Victoria haplochromines (Meier, Sousa, et al. 2017). 10 ...
Within 15,000 years, the explosive adaptive radiation of haplochromine cichlids in Lake Victoria, East Africa, generated 500 endemic species. In the 1980s, the upsurge of Nile perch, a carnivorous fish artificially introduced to the lake, drove the extinction of more than 200 endemic cichlids. The Nile perch predation particularly harmed piscivorous cichlids, including paedophages, cichlids eat eggs and fries, which is an example of the unique trophic adaptation seen in African cichlids. Here, aiming to investigate past demographic events possibly triggered by the invasion of Nile perch and the subsequent impacts on the genetic structure of cichlids, we conducted large-scale comparative genomics. We discovered evidence of recent bottleneck events in four species, including two paedophages, which began during the 1970s–1980s, and population size rebounded during the 1990s-2000s. The timing of the bottleneck corresponded to the historical records of endemic haplochromines’ disappearance and later resurgence, which is likely associated with the introduction of Nile perch by commercial demand to Lake Victoria in the 1950s. Interestingly, among the four species that likely experienced bottleneck, Haplochromis sp. ‘matumbi hunter,’ a paedophagous cichlid, showed the most severe bottleneck signatures. The components of shared ancestry inferred by ADMIXTURE suggested a high genetic differentiation between matumbi hunter and other species. In contrast, our phylogenetic analyses highly supported the monophyly of the five paedophages, consistent with the results of previous studies. We conclude that high genetic differentiation of matumbi hunter occurred due to the loss of shared genetic components among haplochromines in Lake Victoria caused by the recent severe bottleneck.
... Datasets for the bootstrapped replicates were produced by randomly sampling sites with replacement as implemented in the script vcf2sfs.py (Meier et al., 2017;Marques et al., 2019). ...
Early studies of the textbook mixed-ploidy system Biscutella laevigata highlighted diploids restricted to never-glaciated lowlands and tetraploids at high elevations across the European Alps, promoting the hypothesis that whole-genome duplication (WGD) is advantageous under environmental changes. • Climatic niche modelling together with spatial genetics and coalescent modelling based on ddRADseq genotyping of 17 diploid and 19 tetraploid populations was used to revisit the evolution of this species complex in space and time, and to address long-held hypotheses on the role of hybridization at the origin of the tetraploids, their single vs multiple origins, and whether a shift in climatic niche accompanied WGD. • Diploids differentiated into four genetic lineages corresponding to allopatric glacial refugia at the onset of the last ice age, whereas tetraploids displaying tetrasomic inheritance formed a uniform group that originated from southern diploids before the last glacial maximum. Derived from diploids occurring at high-elevation, autotetraploids likely inherited their adaptation to high-elevation rather than having evolved it through or after WGD. They further presented considerable postglacial expansion across the Alps and underwent admixture with diploids. • Although the underpinnings of the successful expansion of autotetraploids remain elusive, differentiation in B. laevigata was chiefly driven by the glacial history in the Alps.
... The downward pyramids of arrows depict multiple generations of hybridization; and (B) the continuation of adaptive radiation, whereby loci affecting ecological adaptation and assortative mating are exchanged and recombined to form novel trait combinations. This can occur through adaptive introgression where a novel trait emerges in one species due to gene flow from another or through hybrid speciation(Meier et al. 2017b) where admixed lineages with new combinations of parental alleles evolve into separate species. ...
Hybridization, or interbreeding between different taxa, was traditionally considered to be rare and to have a largely detrimental impact on biodiversity, sometimes leading to the breakdown of reproductive isolation and even to the reversal of speciation. However, modern genomic and analytical methods have shown that hybridization is common in some of the most diverse clades across the tree of life, sometimes leading to rapid increase of phenotypic variability, to introgression of adaptive alleles, to the formation of hybrid species, and even to entire species radiations. In this review, we identify consensus among diverse research programs to show how the field has progressed. Hybridization is a multifaceted evolutionary process that can strongly influence species formation and facilitate adaptation and persistence of species in a rapidly changing world. Progress on testing this hypothesis will require cooperation among different subdisciplines.
