Introgressive hybridization and natural selection in Darwin's finches

Introgressive hybridization, i.e. hybridization with backcrossing, can lead to the fusion of two species, but it can also lead to evolution of a new trajectory through an enhancement of genetic variation in a new or changed ecological environment. On Daphne Major Island in the Galápagos archipelago, ~1–2% of Geospiza fortis finches breed with the resident G. scandens and with the rare immigrant species G. fuliginosa in each breeding season. Previous research has demonstrated morphological convergence of G. fortis and G. scandens over a 30‐year period as a result of bidirectional introgression. Here we examine the role of hybridization with G. fuliginosa in the evolutionary trajectory of G. fortis. Geospiza fuliginosa (~12 g) is smaller and has a more pointed beak than G. fortis (~17 g). Genetic variation of the G. fortis population was increased by receiving genes more frequently from G. fuliginosa than from G. scandens (~21 g). A severe drought in 2003–2005 resulted in heavy and selective mortality of G. fortis with large beaks, and they became almost indistinguishable morphologically from G. fuliginosa. This was followed by continuing hybridization, a further decrease in beak size and a potential morphological fusion of the two species under entirely natural conditions.     

Introgressive hybridization of tilapias in Zimbabwe

Three species of tilapia native to Zimbabwe, Oreochromis mossambicus, O. mortimeri and O. macrochir are not naturally sympatric, but because of transplantation they have been brought into sympatry. Allozymes of fish examined from Lakes Kariba, Kyle and Chivero showed evidence of introgressive hybridization. The data showed non-random mating populations in Lakes Kariba and Kyle. All three reservoirs displayed individuals with intermediate principal component scores and hybrid index scores indicating hybridization.     

Introgressive hybridization in fishes: the biochemical evidence

Biochemical methods can detect variation at individual genetic loci, making possible the direct assessment of natural hybridization and introgression between fish populations. Protein electro-phoresis has been used to confirm and extend knowledge of many situations where species hybrids have been detected by morphological analyses. New cases of natural hybridization, including some at the subspecies level, have also been identified. Biochemical studies have provided the first conclusive evidence of natural post F₁ hybrids and of introgression between fish taxa. The strongest cases for introgression have used a combined analysis of nuclear protein genes and taxaspecific maternally inherited mitochondrial DNA variation. Information on the significance of introgression as a source of gene flow between taxa, particularly below the species level where sympatric subspecies and sibling species are involved, should expand in the future as the numbers and types of nuclear and mitochondrial DNA loci which can be assayed for variation increase. The full importance of introgressive hybridization in speciation may then be understood.     

Introgressive hybridization of Senecio hercynicus and S. ovatus (Compositae,Senecioneae) along an altitudinal gradient in Harz National Park (Germany)

Introgressive hybridization of Senecio hercynicus and S. ovatus (Compositae, Senecioneae) was studied in a hybrid zone on the southern slopes of Mt Brocken (Harz Mountains, Germany). A total of 415 plants representing 10 stands along an altitudinal gradient were investigated using multivariate statistical analyses of morphological characters and molecular markers (random amplified polymorphic DNA[RAPD]). Both types of traits detected pure S. hercynicus stands on the summit plateau, pure S. ovatus stands at the lowest elevations, and hybrid swarms at intermediate elevations. While morphological and molecular patterns coincided, some individuals in hybrid stands combined morphological patterns typical of S. ovatus with RAPD patterns typical of S. hercynicus, and vice versa. In general, introgression was symmetrical within stands, though one stand combined S. ovatus characters with the glandular hair typical for S. hercynicus, and two stands combined a S. hercynicus typical RAPD genotype with morphological characters shifted towards S. ovatus. Because pure stands of S. hercynicus occurred only on the summit plateau of Mt Brocken, and markers typical for S. ovatus were detectable in stands up to 1040 m a.s.l., future fusion or assimilation of the rare form, S. hercynicus, by the more widespread S. ovatus appears possible at Mt Brocken.     

Introgressive hybridization and evolution of a novel protein phenotype: Glue protein profiles in thenasuta-albomicans complex ofDrosophila

Glue proteins are tissue-specific proteins synthesized by larval salivary gland cells ofDrosophila. InDrosophila nasuta nasuta andD. n. albomicans of thenasuta subgroup, the genes that encode the major glue protein fractions are X-linked. In the present study, these X-linked markers have been employed to trace the pattern of introgression ofD. n. nasuta andD. n. albomicans genomes with respect to the major glue protein fractions in their interracial hybrids, called cytoraces. These cytoraces have inherited the chromosomes of both parents and have been maintained in the laboratory for over 400–550 generations. The analysis has revealed that cytoraces withD. n. albomicans X chromosome show eitherD. n. nasuta pattern or a completely novel pattern of glue protein fractions. Further, quantitative analysis also shows lack of correlation between the chromosomal pattern of inheritance and overall quantity of the major glue protein fractions in the cytoraces. Thus, in cytoraces the parental chromosomes are not just differentially represented but there is evidence for introgression even at the gene level.     

Irrigation and infection: the immunoepidemiology of schistosomiasis in ancient Nubia

Schistosomiasis has been deemed "the most important water-based disease from a global public-health perspective" in modern populations. To better understand the burden of schistosomiasis in ancient populations, we conducted immunologic examinations of desiccated tissue samples from two ancient Nubian populations, Wadi Halfa (N = 46) and Kulubnarti (N = 191). Saqia irrigated agriculture increases the available habitat for the aquatic vector snails and the risk of exposure. On the basis of evidence regarding the impact of saqia irrigation on schistosomiasis prevalence and transmission in modern populations, we predicted that the prevalence of Schistosoma mansoni infection would be higher in Wadi Halfa (saqia irrigation) than Kulubnarti (annual flooding). We also predicted that peak infection prevalence would occur at an earlier age within the Wadi Halfa population than the Kulubnarti population and that in both populations the prevalence of schistosomiasis would be higher in males than females due to differential water contact. The prevalence of S. mansoni was greater in the Wadi Halfa population (26.1%) than at Kulubnarti (9.4%) (P = 0.002). However, peak prevalence of infection did not occur in a younger age category within the Wadi Halfa population; prevalence of infection peaked at 66.7% in the mature adult age group (46+ years) in the Wadi Halfa population and at 16% in the later child age group (6-10 years) in the Kulubnarti population. There were no statistically significant differences in prevalence between males and females of either population. The impact of human alteration of the environment on the transmission of schistosomiasis is clearly shown in these populations.     

Analysis of egg antigens inducing hepatic lesions in schistosome infection

In schistosomiasis, granuloma formation to parasite eggs signals the beginning of a chronic and potentially life-threatening disease. Granulomas are strictly mediated by CD4⁺ T helper (Th) cells specific for egg antigens; however, the number and identity of these T cell-sensitizing molecules are largely unknown. We have used monoclonal T cell reagents as probes to track down, isolate and positively identify several egg antigens; this approach implicitly assures that the molecules of interest are T cell immunogens and, hence, potentially pathogenic. The best-studied egg component is the Sm-p40 antigen. Sm-p40 elicits a strikingly immunodominant Th-1-polarized response in C3H and CBA mice, which are characterized by severe egg-induced immunopathology. Two additional described T cell-sensitizing egg antigens are Schistosoma mansoni phosphoenolpyruvate carboxykinase (Sm-PEPCK) and thioredoxin peroxidase-1 (Sm-TPx-1). In contrast to Sm-p40, both of these molecules induce a more balanced Th-1/Th-2 response, and are relatively stronger antigens in C57BL/6 mice, which develop smaller egg granulomas. Other components, including moieties with molecular weights of 25 kDa (Sm-p25), 150/166 kDa (Sm-p155/166), and 29 kDa (Sm-GST29), are also found to stimulate specific T cells. These findings in the murine model introduce the important notion that egg antigens can vary significantly in immunogenicity according to the host's genetic background. A better knowledge of the principal immunogenic egg components is necessary to ascertain whether such responses can be manipulated for the purpose of reducing pathology.     

Introgressive hybridization erodes morphological divergence between lentic and lotic habitats in an endangered minnow

Introgressive hybridization may erode phenotypic divergence along environmental gradients, collapsing locally adapted populations into a hybrid swarm. Alternatively, introgression may promote phenotypic divergence by providing variation on which natural selection can act. In freshwater fishes, water flow often selects for divergent morphological traits in lake versus stream habitats. We tested the effects of introgression on lake–stream morphological divergence in the minnow Owens Tui Chub (Siphateles bicolor snyderi), which has been rendered endangered by introgession from the introduced Lahontan Tui Chub (Siphateles bicolor obesa). Using geometric morphometric analysis of 457 individual Tui Chub from thirteen populations, we found that both native and introgressing parent taxa exhibited divergent body and caudal fin shapes in lake versus stream habitats, but their trajectories of divergence were distinct. In contrast, introgressed populations exhibited intermediate body and caudal fin shapes that were not differentiated by habitat type, indicating that introgression has eroded phenotypic divergence along the lentic–lotic gradient throughout the historic range of the Owens Tui Chub. Individuals within hybrid populations were less morphologically variable than those within parent populations, suggesting hybrid adaptation to selective agents other than water flow or loss of variance by drift.     

Genetic structure of Schstosoma mansoni in western Kenya: The effects of geography and host sharing

We examined the spatial structure of Schistosoma mansoni, a parasite of humans, from natural infections at two levels: across the Lake Victoria basin of Kenya and among snail hosts. Using 20 microsatellite markers we examined geographic patterns of relatedness and population structure of cercariae and found weak, but significant structure detected by some, but not all analyses. We hypothesise structure created by aggregations of clonal individuals or adherence of hosts to local transmission sites is eroded by high amounts of gene flow in the region. This finding also supports previous hypotheses concerning the evolution of drug resistance in the region. Intrasnail dynamics were investigated in the context of aggregation and kin selection theory to determine how relatedness and also sex influence host sharing and host exploitation. Cercarial production did not differ significantly between snails with one or two genotypes suggesting that mixed infections resulted in decreased individual fitness and provides a framework for reproductive competition. Coinfection patterns in snails were independent of parasite relatedness indicating that schistosomes were not aggregated according to their relatedness and that kin selection was not influencing host sharing. Additionally, host exploitation in coinfections (measured by cercarial production) was not negatively correlated with relatedness, as predicted by classical models due to increased competition and thus exploitation when parasites are unrelated. Because of the low levels of relatedness within the population, schistosomes may rarely encounter close relatives and kin selection mechanisms that influence the distribution of individuals within snails or the virulence mode of the parasites may simply have not evolved.     

Introgressive hybridization between two species of waterstriders (Hemiptera: Gerridae: Limnoporus): geographical structure and temporal change of a hybrid zone

Where the distribution ranges of the waterstriders Limnoporus notabilis and L. dissortis meet in western Canada, extensive hybridization and introgression occurs. Multivariate ordination analyses of genetic and morphometric data by principal component analysis revealed that a single axis separating the two parent species could account for nearly all the variation in both data sets. Maps of principal component scores for both data sets revealed geographical patterns of variation reflecting specific topographic features in the region. Comparisons of morphometric data from some of the samples collected in the 1980s and from the same sites revisited in the 1990s revealed substantial changes. An ‘island’ of dissortis‐like populations inside the range of L. notabilis in interior British Columbia expanded, and a marked local protrusion of notabilis‐like phenotypes into the range of L. dissortis on the east slope of the Rocky Mountains diminished during the decade between collections. We conclude that introgressive hybridization between these two species of waterstriders is a spatially complex and highly dynamic process.     

Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli, Kenya

In 1986, Samuels and Altmann reported evidence for a hybrid zone between Papio anubis and Papio cynocephalus in Amboseli, Kenya, in a baboon population that has been the subject of long-term study since 1971 [Samuels & Altmann, International Journal of Primatology 7:131-138, 1986]. In the current report we document ongoing patterns of hybridization in Amboseli between anubis and yellow baboons. In July 2000, we exhaustively scored living members of study groups for their degree of hybridity, using seven phenotypic characteristics (five in juveniles). We also scored all former members of study groups on the basis of photographic records, field notes, and observer recollections. A total of five anubis males and 11 males with hybrid phenotypes have immigrated into study groups over the course of the long-term study, and immigrations by hybrid males have increased in frequency over time. Further, the increasing frequency of hybrid phenotypes among animals born into study groups indicates that anubis and hybrid males have successfully reproduced in study groups. However, hybrid phenotypes and anubis immigrations were limited to groups in the southwestern portion of the Amboseli basin, with no hybrids occurring in the six eastern groups. Finally, we present evidence that anubis and hybrid males in Amboseli exhibit patterns of natal dispersal that are different from those of yellow males in Amboseli: males with anubis or hybrid phenotypes were significantly more likely to immigrate as juveniles or young subadults than were yellow males.     

Introgressive hybridization as a promoter of genome reshuffling in natural homoploid fish hybrids (Cyprinidae,Leuciscinae)

Understanding the mechanisms underlying diversification and speciation by introgressivehybridization is currently one of the major challenges in evolutionary biology. Here, theanalysis of hybridization between two pairs of Iberian Leuciscinae provided new data onindependent hybrid zones involving Achondrostoma oligolepis (AOL) andPseudochondrostoma duriense (PDU), and confirmed the occurrence of hybridsbetween AOL and Pseudochondrostoma polylepis (PPO). A multilevel survey combiningmorphological, genetic and cytogenomic markers on a vast population screening successfullysorted the selected fishes as admixed. Results were similar in both AOL × PDU andAOL × PPO systems. Overall, hybrid morphotypes, cytogenomic data and geneticprofiling indicated preferential backcrossing and suggested AOL as a major genomiccontributor. Moreover, results implied AOL as more permissive to introgression than PDU orPPO. Although PDU- and PPO-like individuals appeared more resilient to genomemodifications, AOL appeared to be more involved and affected by the ongoing hybridizationevents, as chromosomal translocations were only found in AOL-like individuals. All hybridsanalysed evidenced extensive ribosomal DNA (rDNA) polymorphism that was not found inparental species, but usually seen falling within the range of possible parentalcombinations. Yet, transgressive phenotypes that cannot be explained by normalrecombination, including more rDNA clusters than expected or the occurrence of syntenicrDNAs, were also detected. Present results proved rapid genomic evolution providing thegenetic novelty for species to persist. In addition, although the ultimate consequences ofsuch apparently extensive and recurrent events remain unknown, modern genome-widemethodologies are of great promise towards answering questions concerning the causes,dynamics and impacts of hybridization.     

Bidirectional introgressive hybridization between Lepus capensis and Lepus yarkandensis

Lepus capensis and Lepus yarkandensis are two well-established hare species with different habitat preferences and obvious morphological distinctions. L. capensis is common and widespread while L. yarkandensis is an endemic species with a restricted distribution in the Tarim Basin of western China. During field sampling, individuals with a distinct phenotype were found in the contact zone between the two species. To understand the origin of these unclassified individuals, we analyzed morphological and genetic data from 700 individuals including L. yarkandensis, L. capensis and the unclassified individuals. Morphological analyses of the unclassified individuals revealed that they lie between L. yarkandensis and L. capensis. Genetic analyses based on species-specific molecular markers (mitochondrial control region and SRY) showed that the unclassified populations have mtDNA and SRY genes from both L. capensis and L. yarkandensis, suggesting that the unclassified populations result from hybridization between the two species. Interestingly, many identical and/or very similar mtDNA haplotypes were shared between L. capensis populations and L. yarkandensis populations close to their contact zones, which further suggests the existence of extensive bidirectional mtDNA introgression. Similarly, we found evidence for SRY introgression, though it existed at a lower level compared to mtDNA introgression.     

Introgressive hybridization between Galaxias depressiceps and Galaxias sp D (Teleostei: Galaxiidae) in Otago, New Zealand: Secondary contact mediated by water races

Central Otago (New Zealand) was the focus of an intense period ofgold mining in the late 19th century. Mining relied on high waterpressure for sluicing, often requiring extensive systems of water raceslinking headwaters over large distances. On Rough Ridge, races connectedheadwaters of Otago's two major river systems, the Taieri and theClutha. We employed genetic analysis of freshwater fish(Galaxias) populations to assess the biological implications ofrace-development. The two galaxiid taxa found on Rough Ridge (G. spD and G. depressiceps) are reciprocally monophyletic formtDNA and have three fixed allozyme differences. Rough Ridge aside,G. sp D is apparently absent from the Taieri system and G.depressiceps from the Clutha system. Distributions of mitochondrialDNA, allozyme and microsatellite alleles imply that artificialconnections have facilitated bidirectional introgression: movementof G. sp D alleles into the Taieri system and G.depressiceps alleles into the Clutha. The finding of some identicalcontrol region haplotypes (of both lineages) on either side of thecatchment boundary confirms the recency of genetic exchange. Near theinferred region of contact, samples from Linn Burn (Taieri) are pureG. depressiceps for three diagnostic allozymes and mtDNA.Samples from upper Pool Burn (Clutha) are pure G. sp D forthese same four markers. However, other collections from around thecontact zone represent genetic mixtures forming a cline. We fear thatsimilar human-induced mixing may have happened elsewhere in uplandOtago.     

Introduction. Extent, processes and evolutionary impact of interspecific hybridization in animals

Since the time of Charles Darwin, studies of interspecific hybridization have been a major focus for evolutionary biologists. Although this phenomenon has often been viewed as problematic in the fields of ecology, taxonomy and systematics, it has become a primary source of data for studies on speciation and adaptation. Effects from genetic/evolutionary processes, such as recombination and natural selection, usually develop over extended periods of time; however, they are accelerated in cases of hybridization. Interspecific hybrids exhibit novel genomes that are exposed to natural selection, thus providing a key to unravel the ultimate causes of adaptation and speciation. Here we provide firstly a historic perspective of hybridization research, secondly a novel attempt to assess the extent of hybridization among animals and thirdly an overview of the reviews and case studies presented in this theme issue.     

Differential selection to avoid hybridization in two toad species

Abstract.— The fitness consequences of hybridization critically affect the speciation process. When hybridization is costly, selection favors the evolution of prezygotic isolating mechanisms (e.g., mating behaviors) that reduce heter-ospecific matings and, consequently, enhance reproductive isolation between species (a process termed reinforcement). If, however, selection to avoid hybridization differs between species, reinforcement may be impeded. Here, we examined both the frequency and fitness effects of hybridization between plains spadefoot toads ( Spea bombifrons ) and New Mexico spadefoot toads ( S. multiplicata ). Hybridization was most frequent in smaller breeding ponds that tend to be ephemeral, and heterospecific pairs consisted almost entirely of S. bombifrons females and S. multiplicata males. Moreover, in controlled experimental crosses, hybrid offspring from crosses in which S. multiplicata was maternal had significantly lower survival and longer development time than pure S. multiplicata offspring. By contrast, hybrid offspring from crosses in which S. bombifrons was maternal outperformed pure S. bombifrons offspring by reaching metamorphosis faster. These data suggest that, although S. multiplicata females are under selection to avoid hybridization, selection might favor those S. bombifrons females that hybridize with S. multiplicata if their breeding pond is highly ephemeral. Generally, the strength of selection to avoid hybridization may differ for hybridizing species, possibly impeding reinforcement.     

Molecular and morphological evidence of hybridization between newts Triturus vulgaris and T. montandoni (Caudata: Salamandridae) in Slovakia

Natural hybridization and introgression is recorded between the newt species Triturus vulgaris and T. montandoni in Slovakia. To confirm a hybrid status of two putative hybrids, morphological and Randomly Amplified Polymorphic DNA (RAPD) markers specific for T. vulgaris and T. montandoni were used. The individuals found in Zbojská (Veporské vrchy Mts, Slovakia; analyzed morphologically and genetically) and Zubrohlava (Oravská kotlina basin, Slovakia; analyzed only morphologically) possessed markers of both species. Segregation of RAPD markers together with a model-based Bayesian analysis revealed that the specimen from Zbojská belonged to later generation hybrids.     

Introgressive hybridization facilitates adaptive divergence in a recent radiation of monkeyflowers

A primary goal in evolutionary biology is to identify the historical events that have facilitated the origin and spread of adaptations. When these adaptations also lead to reproductive isolation, we can learn about the evolutionary mechanisms contributing to speciation. We reveal the complex history of the gene MaMyb2 in shaping flower colour divergence within a recent radiation of monkeyflowers. In the Mimulus aurantiacus species complex, red-flowered M. a. ssp. puniceus and yellow-flowered M. a. ssp. australis are partially isolated because of differences in pollinator preferences. Phylogenetic analyses based on genome-wide variation across the complex suggest two origins of red flowers from a yellow-flowered ancestor: one in M. a. ssp. puniceus and one in M. a. ssp. flemingii. However, in both cases, red flowers are caused by cis-regulatory mutations in the gene MaMyb2. Although this could be due to distinct mutations in each lineage, we show that the red allele in M. a. ssp. puniceus did not evolve de novo or exist as standing variation in its yellow-flowered ancestor. Rather, our results suggest that a single red MaMyb2 allele evolved during the radiation of M. aurantiacus that was subsequently transferred to the yellow-flowered ancestor of M. a. ssp. puniceus via introgressive hybridization. Because gene flow is still possible among taxa, we conclude that introgressive hybridization can be a potent driver of adaptation at the early stages of divergence that can contribute to the origins of biodiversity.     

Efficient linkage mapping using exome capture and extreme QTL in schistosome parasites

Background

Identification of parasite genes that underlie traits such as drug resistance and host specificity is challenging using classical linkage mapping approaches. Extreme QTL (X-QTL) methods, originally developed by rodent malaria and yeast researchers, promise to increase the power and simplify logistics of linkage mapping in experimental crosses of schistosomes (or other helminth parasites), because many 1000s of progeny can be analysed, phenotyping is not required, and progeny pools rather than individuals are genotyped. We explored the utility of this method for mapping a drug resistance gene in the human parasitic fluke Schistosoma mansoni.

Results

We staged a genetic cross between oxamniquine sensitive and resistant parasites, then between two F1 progeny, to generate multiple F2 progeny. One group of F2s infecting hamsters was treated with oxamniquine, while a second group was left untreated. We used exome capture to reduce the size of the genome (from 363 Mb to 15 Mb) and exomes from pooled F2 progeny (treated males, untreated males, treated females, untreated females) and the two parent parasites were sequenced to high read depth (mean = 95-366×) and allele frequencies at 14,489 variants compared. We observed dramatic enrichment of alleles from the resistant parent in a small region of chromosome 6 in drug-treated male and female pools (combined analysis: = 11.07, p = 8.74 × 10^-29). This region contains Smp_089320 a gene encoding a sulfotransferase recently implicated in oxamniquine resistance using classical linkage mapping methods.

Conclusions

These results (a) demonstrate the utility of exome capture for generating reduced representation libraries in Schistosoma mansoni, and (b) provide proof-of-principle that X-QTL methods can be successfully applied to an important human helminth. The combination of these methods will simplify linkage analysis of biomedically or biologically important traits in this parasite.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-617) contains supplementary material, which is available to authorized users.