scholarly journals Asymmetric Reproductive Barriers and Gene Flow Promote the Rise of a Stable Hybrid Zone in the Mediterranean High Mountain

2021 ◽  
Vol 12 ◽  
Author(s):  
Mohamed Abdelaziz ◽  
A. Jesús Muñoz-Pajares ◽  
Modesto Berbel ◽  
Ana García-Muñoz ◽  
José M. Gómez ◽  
...  

Hybrid zones have the potential to shed light on evolutionary processes driving adaptation and speciation. Secondary contact hybrid zones are particularly powerful natural systems for studying the interaction between divergent genomes to understand the mode and rate at which reproductive isolation accumulates during speciation. We have studied a total of 720 plants belonging to five populations from two Erysimum (Brassicaceae) species presenting a contact zone in the Sierra Nevada mountains (SE Spain). The plants were phenotyped in 2007 and 2017, and most of them were genotyped the first year using 10 microsatellite markers. Plants coming from natural populations were grown in a common garden to evaluate the reproductive barriers between both species by means of controlled crosses. All the plants used for the field and greenhouse study were characterized by measuring traits related to plant size and flower size. We estimated the genetic molecular variances, the genetic differentiation, and the genetic structure by means of the F-statistic and Bayesian inference. We also estimated the amount of recent gene flow between populations. We found a narrow unimodal hybrid zone where the hybrid genotypes appear to have been maintained by significant levels of a unidirectional gene flow coming from parental populations and from weak reproductive isolation between them. Hybrid plants exhibited intermediate or vigorous phenotypes depending on the analyzed trait. The phenotypic differences between the hybrid and the parental plants were highly coherent between the field and controlled cross experiments and through time. The highly coherent results obtained by combining field, experimental, and genetic data demonstrate the existence of a stable and narrow unimodal hybrid zone between Erysimum mediohispanicum and Erysimum nevadense at the high elevation of the Sierra Nevada mountains.

Author(s):  
Linda Hagberg ◽  
Enrique Celemin ◽  
Iker Irisarri ◽  
Oliver Hawlitschek ◽  
J L Bella ◽  
...  

Although the process of species formation is notoriously idiosyncratic, the observation of pervasive patterns of reproductive isolation across species pairs suggests that generalities, or “rules”, underlie species formation in all animals. Haldane’s rule states that whenever a sex is absent, rare or sterile in a cross between two taxa, that sex is usually the heterogametic sex. Yet, understanding how Haldane’s rule first evolves and whether it is associated to genome wide barriers to gene flow remains a challenging task because this rule is usually studied in highly divergent taxa that no longer hybridize in nature. Here, we address these questions using the meadow grasshopper Pseudochorthippus parallelus where populations that readily hybridize in two natural hybrid zones show hybrid male sterility in laboratorial crosses. Using mitochondrial data, we infer that such populations have diverged some 100,000 years ago, surviving multiple glacial periods in isolated Pleistocenic refugia. Nuclear data shows that secondary contact has led to extensive introgression throughout the species range, including between populations showing hybrid male sterility. We find repeatable patterns of genomic differentiation across the two hybrid zones, yet such patterns are consistent with shared genomic constraints across taxa rather than their role in reproductive isolation. Together, our results suggest that Haldane’s rule can evolve relatively quickly within species, particularly when associated to strong demographic changes. At such early stages of species formation, hybrid male sterility still permits extensive gene flow, allowing future studies to identify genomic regions associated with reproductive barriers.


2019 ◽  
Author(s):  
I. van Riemsdijk ◽  
J.W. Arntzen ◽  
G. Bucciarelli ◽  
E. McCartney-Melstad ◽  
M. Rafajlović ◽  
...  

AbstractThe barrier effect is a restriction of gene flow between diverged populations by barrier genes. Restriction of gene flow and asymmetric introgression over multiple transects indicates species wide (genetic) adaptations, whereas transect-specific barrier loci may indicate local adaptation to gene flow. Asymmetric introgression can be caused by selection, hybrid zone movement, asymmetric reproductive isolation, or a combination of these. We study two widely separated transects (northwest and southeast France) for the 900 km long hybrid zone between Bufo bufo and B. spinosus toads, using ~1200 markers from restriction-site associated DNA (RAD) sequencing data. Genomic and geographic clines were used to identify outlier markers which show restricted or elevated introgression. Twenty-six barrier markers are shared between transects (the union of 56 and 123 barrier markers identified in each transect), which is more than would be expected by chance. However, the number of barrier markers is twice as high in the southeast transect. In the northwest transect a high amount of (asymmetric) introgression from B. spinosus into B. bufo is consistent with hybrid zone movement or asymmetric reproductive isolation. In the southeast transect, introgression is symmetric and consistent with a stable hybrid zone. Differences between transects may be related to genetic sub-structure within B. bufo. A longer period of secondary contact in southeast France appears to result in a relatively stronger barrier effect than in the northwest. The Bufo hybrid zone provides an excellent opportunity to separate a general barrier to gene flow from local reductions in gene flow.


Behaviour ◽  
2015 ◽  
Vol 152 (14) ◽  
pp. 1933-1951 ◽  
Author(s):  
Tamsin Burbidge ◽  
Thari Parson ◽  
Paula C. Caycedo-Rosales ◽  
Carlos Daniel Cadena ◽  
Hans Slabbekoorn

Behavioural barriers to gene flow can play a key role in speciation and hybridisation. Birdsong is well-known for its potential contribution to such behavioural barriers as it may affect gene flow through an effect on territorial and mating success across population boundaries. Conspecific recognition and heterospecific discrimination of acoustic variation can prevent or limit hybridization in areas where closely related species meet. Here we tested the impact of song differences on territorial response levels between two adjacent Henicorhina wood-wren species along an elevational gradient in Colombia. In an earlier study, playback results had revealed an asymmetric response pattern, with low-elevation H. leucophrys bangsi responding strongly to any conspecific or heterospecific song variant, whereas high-elevation H. anachoreta birds discriminated, responding more strongly to their own songs than to those of bangsi. However, in that study we could not exclude a role for relative familiarity to the song stimuli. In the current study we confirm the asymmetric response pattern with song stimuli recorded close to and on both sides of the distinct acoustic boundary. Furthermore, we also show a previously unnoticed divergence in singing style between these two wood-wren species, which may contribute to an acoustically guided barrier to hybridization in this secondary contact zone.


Genetics ◽  
1990 ◽  
Vol 124 (4) ◽  
pp. 921-936 ◽  
Author(s):  
J Mallet ◽  
N Barton ◽  
G Lamas ◽  
J Santisteban ◽  
M Muedas ◽  
...  

Abstract Hybrid zones can yield estimates of natural selection and gene flow. The width of a cline in gene frequency is approximately proportional to gene flow (sigma) divided by the square root of per-locus selection (square root of s). Gene flow also causes gametic correlations (linkage disequilibria) between genes that differ across hybrid zones. Correlations are stronger when the hybrid zone is narrow, and rise to a maximum roughly equal to s. Thus cline width and gametic correlations combine to give estimates of gene flow and selection. These indirect measures of sigma and s are especially useful because they can be made from collections, and require no field experiments. The method was applied to hybrid zones between color pattern races in a pair of Peruvian Heliconius butterfly species. The species are Müllerian mimics of one another, and both show the same changes in warning color pattern across their respective hybrid zones. The expectations of cline width and gametic correlation were generated using simulations of clines stabilized by strong frequency-dependent selection. In the hybrid zone in Heliconius erato, clines at three major color pattern loci were between 8.5 and 10.2 km wide, and the pairwise gametic correlations peaked at R approximately 0.35. These measures suggest that s approximately 0.23 per locus, and that sigma approximately 2.6 km. In erato, the shapes of the clines agreed with that expected on the basis of dominance. Heliconius melpomene has a nearly coincident hybrid zone. In this species, cline widths at four major color pattern loci varied between 11.7 and 13.4 km. Pairwise gametic correlations peaked near R approximately 1.00 for tightly linked genes, and at R approximately 0.40 for unlinked genes, giving s approximately 0.25 per locus and sigma approximately 3.7 km. In melpomene, cline shapes did not perfectly fit theoretical shapes based on dominance; this deviation might be explained by long-distance migration and/or strong epistasis. Compared with erato, sample sizes in melpomene are lower and the genetics of its color patterns are less well understood. In spite of these problems, selection and gene flow are clearly of the same order of magnitude in the two species. The relatively high per locus selection coefficients agree with "major gene" theories for the evolution of Müllerian mimicry, but the genetic architecture of the color patterns does not. These results show that the genetics and evolution of mimicry are still only sketchily understood.


2020 ◽  
Author(s):  
Ailene MacPherson ◽  
Silu Wang ◽  
Ryo Yamaguchi ◽  
Loren H. Riesesberg ◽  
Sarah P. Otto

AbstractPopulation genomic analysis of hybrid zones is instrumental to our understanding of the evolution of reproductive isolation. Many temperate hybrid zones are formed by the secondary contact between two parental populations that had undergone post-glacial range expansion. Here we show that explicitly accounting for historical parental isolation followed by range expansion prior to secondary contact is fundamental for explaining genetic and fitness patterns in these hybrid zones. Specifically, ancestral population expansion can result in allele surfing, neutral or slightly deleterious mutations drift high frequency at the front of the expansion. If these surfed deleterious alleles are recessive, they can contribute to substantial heterosis in hybrids produced at secondary contact, counteracting negative-epistatic interactions between BDMI loci and hence can deteriorate reproductive isolation. Similarly, surfing at neutral loci can alter the expected pattern of population ancestry and suggests that accounting for historical population expansion is necessary to develop accurate null genomic models in secondary-contact hybrid zones. Furthermore, this process should be incorporated in macroevolutionary models of divergence as well, since such heterosis facilitated by parental-range expansion could dampen genomic divergence established in the past.


2017 ◽  
Author(s):  
Brandon S. Cooper ◽  
Alisa Sedghifar ◽  
W. Thurston Nash ◽  
Aaron A. Comeault ◽  
Daniel R. Matute

ABSTRACTGeographical areas where two species come into contact and hybridize serve as natural laboratories for assessing mechanisms that limit gene flow between species. The ranges of about half of all closely related Drosophila species overlap, and the genomes of several pairs reveal signatures of past introgression. However, only two contemporary hybrid zones have been characterized in the genus, and both are recently diverged sister species (D. simulans-D. sechellia, Ks = 0.05; D. yakuba-D. santomea, Ks = 0.048). Here we present evidence of a new hybrid zone, and the ecological mechanisms that maintain it, between two highly divergent Drosophila species (Ks = 0.11). On the island of Bioko in west Africa, D. teissieri occupies mostly forests, D. yakuba occupies mostly open agricultural areas, and recently, we discovered that hybrids between these species occur near the interface of these habitats. Genome sequencing revealed that all field-sampled hybrids are F1 progeny of D. yakuba females and D. teissieri males. We found no evidence for either advanced-generation hybrids or F1 hybrids produced by D. teissieri females and D.yakuba males. The lack of advanced-generation hybrids on Bioko is consistent with mark-recapture and laboratory experiments that we conducted, which indicate hybrids have a maladaptive combination of traits. Like D. yakuba, hybrids behaviorally prefer open habitat that is relatively warm and dry, but like D. teissieri, hybrids have low desiccation tolerance, which we predict leaves them physiologically ill-equipped to cope with their preferred habitat. These observations are consistent with recent findings of limited introgression in the D. yakuba clade and identify an ecological mechanism for limiting gene flow between D. yakuba and D. teissieri; namely, selection against hybrids that we have documented, in combination with hybrid male sterility, contributes to the maintenance of this narrow (~30m), stable hybrid zone centered on the forest-open habitat ecotone. Our results show how a deleterious combination of parental traits can result in unfit or maladapted hybrids.


2009 ◽  
Vol 8 (2) ◽  
pp. 326-333 ◽  
Author(s):  
Robert W. Derlet ◽  
Charles R. Goldman ◽  
Michael J. Connor

The Sierra Nevada Mountain range serves as an important source of drinking water for the State of California. However, summer cattle grazing on federal lands affects the overall water quality yield from this essential watershed as cattle manure is washed into the lakes and streams or directly deposited into these bodies of water. This organic pollution introduces harmful microorganisms and also provides nutrients such as nitrogen and phosphorus which increase algae growth causing eutrophication of otherwise naturally oligotrophic mountain lakes and streams. Disinfection and filtration of this water by municipal water districts after it flows downstream will become increasingly costly. This will be compounded by increasing surface water temperatures and the potential for toxins release by cyanobacteria blooms. With increasing demands for clean water for a state population approaching 40 million, steps need to be implemented to mitigate the impact of cattle on the Sierra Nevada watershed. Compared to lower elevations, high elevation grazing has the greatest impact on the watershed because of fragile unforgiving ecosystems. The societal costs from non-point pollution exceed the benefit achieved through grazing of relatively few cattle at the higher elevations. We propose limiting summer cattle grazing on public lands to lower elevations, with a final goal of allowing summer grazing on public lands only below 1,500 m elevation in the Central and Northern Sierra and 2,000 m elevation in the Southern Sierra.


1967 ◽  
Vol 24 (8) ◽  
pp. 1637-1692 ◽  
Author(s):  
D. W. Hagen

A systematic examination was made of isolating mechanisms, as set out by Mayr, that might serve to maintain reproductive isolation between the marine (trachurus) and the freshwater (leiurus) threespine sticklebacks. Field work was conducted in a small British Columbia coastal stream, the Little Campbell River, for[Formula: see text] years and complemented with laboratory experiments. Other streams were included late in the investigation. Leiurus permanently occupies the upper reaches of the stream; trachurus is anadromous and enters the lower reaches to breed in freshwater. Between the breeding grounds of the two, where numbers of both are greatly reduced, hybridization occurs. But it is restricted to a narrow zone.The two species are easily distinguished. Thus, morphological analysis provided firm circumstantial evidence that hybrids are plentiful and that backcrossing occurs, predominately to leiurus. Hybridization was confirmed by rearing offspring under uniform conditions in the laboratory with crosses in all combinations. Such offspring were also used to demonstrate considerable genetic divergence (much of it polygenetic) between leiurus and trachurus.Behavioural experiments demonstrated the absence of ethological isolation and hybrids performed courtship and parental care normally.Nor was genetic incompatibility found in the reared hybrids (F1's or backcrosses); all were vigourous. Seasonal isolation is only partially developed with early spawning migrants of trachurus making a major contribution to hybridization (in the Little Campbell River).Since behavioural and genetic blocks to hybridization are not present, there is no means to prevent hybridization where leiurus and trachurus come together. However, coexistence between the two species is very low. Evidence from observation and experiment in the field and from preference tests showed that ecological isolation is a very powerful barrier to hybridization. The two species show numerous adaptations to the distinctly different habitats they frequent, and each shows a strong affinity for its own habitat. In localities with intermediate or contiguous habitats, coexistence and interbreeding occur. Hybridization is a function of the environment.No selection against hybrids could be detected within the hybrid zone (or with laboratory reared hybrids); yet, one is forced to assume that it is present outside the zone. The very narrow zones as well as the reversed cline that were found indicate there is intense selection against hybrids. What these selective forces are remains to be found. Hybrid zones will probably continue to be poorly understood until a critical analysis of hybrid inferiority is made.Genotypes of either species that remain in the hybrid zone are at a strong selective disadvantage. Hence, reinforcement of ecological isolation probably occurs, and Moore's criticism concerning the spread of such reinforced genotypes would not apply to such cases. Mayr distinguishes between pre- and postmating mechanisms stating that the mode of operation of natural selection will be different for the two. But in threespine sticklebacks one premating mechanism (ecological isolation) and one postmating mechanism (hybrid inferiority) cannot be distinguished. This is so because ecological isolation is the cause of hybrid inferiority.Leiurus and trachurus are reproductively isolated, have well developed isolating mechanisms, and exhibit considerable genetic divergence. The two, then, fulfill the species definition of Mayr. There is no evidence that introgression occurs. Indeed a reversed cline showing a progressive increase in morphological divergence between the two species as the hybrid zone is approached together with the narrow hybrid zone demonstrates that selection severely restricts gene flow. Collections and observations from other streams corroborate those from the study area. Reproductive isolation between leiurus and trachurus seems to be widespread, throughout their range.


2014 ◽  
Vol 281 (1776) ◽  
pp. 20132733 ◽  
Author(s):  
Yasmin Latour ◽  
Marco Perriat-Sanguinet ◽  
Pierre Caminade ◽  
Pierre Boursot ◽  
Carole M. Smadja ◽  
...  

Sexual selection may hinder gene flow across contact zones when hybrid recognition signals are discriminated against. We tested this hypothesis in a unimodal hybrid zone between Mus musculus musculus and Mus musculus domesticus where a pattern of reinforcement was described and lower hybrid fitness documented. We presented mice from the border of the hybrid zone with a choice between opposite sex urine from the same subspecies versus hybrids sampled in different locations across the zone. While no preference was evidenced in domesticus mice, musculus males discriminated in favour of musculus signals and against hybrid signals. Remarkably, the pattern of hybrid unattractiveness did not vary across the hybrid zone. Moreover, allopatric populations tested in the same conditions did not discriminate against hybrid signals, indicating character displacement for signal perception or preference. Finally, habituation–discrimination tests assessing similarities between signals pointed out that hybrid signals differed from the parental ones. Overall, our results suggest that perception of hybrids as unattractive has evolved in border populations of musculus after the secondary contact with domesticus . We discuss the mechanisms involved in hybrid unattractiveness, and the potential impact of asymmetric sexual selection on the hybrid zone dynamics and gene flow between the two subspecies.


2019 ◽  
Vol 110 (5) ◽  
pp. 523-534 ◽  
Author(s):  
Brendan J Pinto ◽  
James Titus-McQuillan ◽  
Juan D Daza ◽  
Tony Gamble

Abstract Determining the mechanisms that create and maintain biodiversity is a central question in ecology and evolution. Speciation is the process that creates biodiversity. Speciation is mediated by incompatibilities that lead to reproductive isolation between divergent populations and these incompatibilities can be observed in hybrid zones. Gecko lizards are a speciose clade possessing an impressive diversity of behavioral and morphological traits. In geckos, however, our understanding of the speciation process is negligible. To address this gap, we used genetic sequence data (both mitochondrial and nuclear markers) to revisit a putative hybrid zone between Sphaerodactylus nicholsi and Sphaerodactylus townsendi in Puerto Rico, initially described in 1984. First, we addressed discrepancies in the literature on the validity of both species. Second, we sampled a 10-km-wide transect across the putative hybrid zone and tested explicit predictions about its dynamics using cline models. Third, we investigated potential causes for the hybrid zone using species distribution modeling and simulations; namely, whether unique climatic variables within the hybrid zone might elicit selection for intermediate phenotypes. We find strong support for the species-level status of each species and no evidence of movement, or unique climatic variables near the hybrid zone. We suggest that this narrow hybrid zone is geographically stable and is maintained by a combination of dispersal and selection. Thus, this work has identified an extant model system within geckos that that can be used for future investigations detailing genetic mechanisms of reproductive isolation in an understudied vertebrate group.


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