Evolutionary Consequences Of Hybridization Research Articles

Demographic history and species delimitation of threeZamiaspecies (Zamiaceae) in south-eastern Mexico:Z. katzerianais not a product of hybridization

AbstractSpeculations on hybridization among wild cycads are abundant, but empirical evidence of hybridization in cycad evolution is almost non-existent and the evolutionary consequences of hybridization in cycads have not been discussed. Previously, Zamia katzeriana was hypothesized to have a hybrid origin between two sympatric species: Z. splendens and Z. loddigesii. In this study, we aimed to reveal whether such a hypothesis is confirmed. Variation in 12 microsatellite loci, 12 morphological traits and environmental niche of ten populations representing the three species was examined. Gene flow and scenarios of demographic history were tested. Ecological niche models were reconstructed to examine present and past niche availability of the two putative parental species. Correlations between genetic, morphological, environmental and geographical distances were tested. We found that Z. katzeriana diverged from Z. splendens without experiencing admixture with its sympatric congeners. However, gene flow between Z. splendens and Z. loddigesii has occurred in one locality. The niches of the two latter species have overlapped since the Last Glacial Maximum, when admixture probably occurred. However, the admixed populations do not resemble Z. katzeriana. These results confirm that Z. katzeriana did not originate from hybridization between Z. splendens and Z. loddigesii.

Genomic insights into hybridization of reef corals

Hybridization plays a fundamental role in speciation and diversification of plants and animals. Hybridization among highly diverse assemblages of reef corals is well known and widely reported, but the ecological and evolutionary consequences of hybridization among reef corals are only just beginning to become apparent. In this perspective, I introduce introgression and polyploidy in the hybridization (reticulate evolution) of reef corals and then discuss the roles of hybridization in the evolution of Acropora with recent genomic evidence. Finally, I discuss how advances of genomics will facilitate the study of hybridization in reef corals. Together, understanding the genomic basis of reef coral hybridization provides new insights into coral resilience, as well as coral reef biodiversity and conservation.

Interspecific hybridization can generate functional novelty in cichlid fish.

The role of interspecific hybridization in evolution is still being debated. Interspecific hybridization has been suggested to facilitate the evolution of ecological novelty, and hence the invasion of new niches and adaptive radiation when ecological opportunity is present beyond the parental species niches. On the other hand, hybrids between two ecologically divergent species may perform less well than parental species in their respective niches because hybrids would be intermediate in performance in both niches. The evolutionary consequences of hybridization may hence be context-dependent, depending on whether ecological opportunities, beyond those of the parental species, do or do not exist. Surprisingly, these complementary predictions may never have been tested in the same experiment in animals. To do so, we investigate if hybrids between ecologically distinct cichlid species perform less well than the parental species when feeding on food either parent is adapted to, and if the same hybrids perform better than their parents when feeding on food none of the species are adapted to. We generated two first-generation hybrid crosses between species of African cichlids. In feeding efficiency experiments we measured the performance of hybrids and parental species on food types representing both parental species niches and additional 'novel' niches, not used by either of the parental species but by other species in the African cichlid radiations. We found that hybrids can have higher feeding efficiencies on the 'novel' food types but typically have lower efficiencies on parental food types when compared to parental species. This suggests that hybridization can generate functional variation that can be of ecological relevance allowing the access to resources outside of either parental species niche. Hence, we provide support for the hypothesis of ecological context-dependency of the evolutionary impact of interspecific hybridization.

Genomic evidence of hybridization between two independent invasions of European green crab (Carcinus maenas) in the Northwest Atlantic.

Invasive species have been associated with significant negative impacts in their introduced range often outcompeting native species, yet the long-term evolutionary dynamics of biological invasions are not well understood. Hybridization, either among waves of invasion or between native and introduced populations, could alter the ecological and evolutionary impacts of invasions yet has rarely been studied in marine invasive species. The European green crab (Carcinus maenas) invaded eastern North America twice from northern and southern locations in its native range. Here we examine the frequency of hybridization among these two distinct invasions at locations from New Jersey, USA to Newfoundland, Canada using restriction-site-associated DNA sequencing (RAD-seq), microsatellite loci and cytochrome c oxidase subunit I mitochondrial DNA (mtDNA) sequences. We used Bayesian clustering and hybrid assignment analyses to investigate hybridization between the northern and southern populations. Of the samples analyzed, six locations contained at least one hybrid individual, while two locations were characterized by extensive hybridization, with 95% of individuals collected from Placentia Bay, Newfoundland being hybrids (mostly F2) and 90% of individuals from Kejimkujik, Nova Scotia being classified as hybrids, mostly backcrosses to the northern ecotype. The presence of both F2 hybrids and backcrossed individuals suggests that these hybrids are viable and introgression is occurring between invasions. Our results provide insight into the demographic and evolutionary consequences of hybridization between independent invasions, and will inform the management of green crabs in eastern North America.

Hybridization in Plants: Old Ideas, New Techniques.

Hybridization has played an important role in the evolution of many lineages. With the growing availability of genomic tools and advancements in genomic analyses, it is becoming increasingly clear that gene flow between divergent taxa can generate new phenotypic diversity, allow for adaptation to novel environments, and contribute to speciation. Hybridization can have immediate phenotypic consequences through the expression of hybrid vigor. On longer evolutionary time scales, hybridization can lead to local adaption through the introgression of novel alleles and transgressive segregation and, in some cases, result in the formation of new hybrid species. Studying both the abundance and the evolutionary consequences of hybridization has deep historical roots in plant biology. Many of the hypotheses concerning how and why hybridization contributes to biological diversity currently being investigated were first proposed tens and even hundreds of years ago. In this Update, we discuss how new advancements in genomic and genetic tools are revolutionizing our ability to document the occurrence of and investigate the outcomes of hybridization in plants.

Hybridization and back-crossing in giant petrels (Macronectes giganteus and M. halli) at Bird Island, South Georgia, and a summary of hybridization in seabirds.

Hybridization in natural populations provides an opportunity to study the evolutionary processes that shape divergence and genetic isolation of species. The emergence of pre-mating barriers is often the precursor to complete reproductive isolation. However, in recently diverged species, pre-mating barriers may be incomplete, leading to hybridization between seemingly distinct taxa. Here we report results of a long-term study at Bird Island, South Georgia, of the extent of hybridization, mate fidelity, timing of breeding and breeding success in mixed and conspecific pairs of the sibling species, Macronectes halli (northern giant petrel) and M. giganteus (southern giant petrel). The proportion of mixed-species pairs varied annually from 0.4–2.4% (mean of 1.5%), and showed no linear trend with time. Mean laying date in mixed-species pairs tended to be later than in northern giant petrel, and always earlier than in southern giant petrel pairs, and their breeding success (15.6%) was lower than that of conspecific pairs. By comparison, mixed-species pairs at both Marion and Macquarie islands always failed before hatching. Histories of birds in mixed-species pairs at Bird Island were variable; some bred previously or subsequently with a conspecific partner, others subsequently with a different allospecific partner, and some mixed-species pairs remained together for multiple seasons. We also report the first verified back-crossing of a hybrid giant petrel with a female northern giant petrel. We discuss the potential causes and evolutionary consequences of hybridization and back-crossing in giant petrels and summarize the incidence of back-crossing in other seabird species.

Gene mapping of 28S and 5S rDNA sites in chromosomes of two Barbus species and their F1 hybrids (Teleostei, Cyprinidae)

Gene mapping of 28S and 5S rDNA sites in chromosomes of two Barbus species and their F1 hybrids (Teleostei, Cyprinidae)

Hierarchical behaviour, habitat use and species size differences shape evolutionary outcomes of hybridization in a coral reef fish.

Hybridization is an important evolutionary process, with ecological and behavioural factors influencing gene exchange between hybrids and parent species. Patterns of hybridization in anemonefishes may result from living in highly specialized habitats and breeding status regulated by size-based hierarchal social groups. Here, morphological, ecological and genetic analyses in Kimbe Bay, Papua New Guinea, examine the hybrid status of Amphiprion leucokranos, a nominal species and presumed hybrid between Amphiprion sandaracinos and Amphiprion chrysopterus. We test the hypothesis that habitat use and relative size differences of the parent species and hybrids determine the patterns of gene exchange. There is strong evidence that A.leucokranos is a hybrid of smaller A.sandaracinos and larger A.chrysopterus, where A.chrysopterus is exclusively the mother to each hybrid, based on mtDNA cytochrome b and multiple nDNA microsatellite loci. Overlap in habitat, depth and host anemone use was found, with hybrids intermediate to parents and cohabitation in over 25% of anemones sampled. Hybrids, intermediate in body size, colour and pattern, were classified 55% of the time as morphologically first-generation hybrids relative to parents, whereas 45% of hybrids were more A.sandaracinos-like, suggesting backcrossing. Unidirectional introgression of A.chrysopterus mtDNA into A.sandaracinos via hybrid backcrosses was found, with larger female hybrids and small male A.sandaracinos mating. Potential nDNA introgression was also evident through distinct intermediate hybrid genotypes penetrating both parent species. Findings support the hypothesis that anemonefish hierarchical behaviour, habitat use and species-specific size differences determine how hybrids form and the evolutionary consequences of hybridization.

Hybridization of two ancient salamander lineages: molecular evidence for endemic spectacled salamanders on the Apennine peninsula

Current studies indicate that both processes and mechanisms of natural hybridization go far beyond the formation and maintenance of hybrid zones between species. These studies demonstrate that the evolutionary consequences of hybridization can include extinction or extirpation of lineages but may also favor the formation of new hybrid species in an ecological context. The unambiguous identification of occurrences of hybridization in natural populations is a crucial first step in addressing questions related to natural hybridization in both evolutionary and ecological terms. Here, we provide the first molecular evidence of extensive natural hybridization between two ancient sister species of spectacled salamanders - Salamandrina perspicillata in northern and Salamandrina terdigitata in southern Italy. Parental lineages diverged at least 10 million years ago during the Lower Pliocene and represent the most ancient split between any congeneric amphibian species endemic to the Italian peninsula. Analysis of the mitochondrial cytochrome b (Cyt b), nuclear-encoded recombination-activating protein (RAG-1) and propriomelano-cortin (POMC) genes of more than 250 individuals from populations of both species and from the contact zone, show clear evidence of ongoing hybridization. Whereas 20% of the individuals from the contact population showed no signs of hybridization for the applied markers, the remainder (80%) were identified as first generation hybrids and backcrossed individuals. Our results suggest that hybridization between these two ancient lineages produces viable and fertile offspring, highlighting the need for research on possible mechanisms that prevent the intermixing and hybridization of parental species on a broader geographical scale.

Variable patterns of introgression in two sculpin hybrid zones suggest that genomic isolation differs among populations

Theory predicts that reproductive isolation may be due to intrinsic genetic incompatibilities or extrinsic ecological factors. Therefore, an understanding of the genetic basis of isolation may require analyses of evolutionary processes in situ to include environmental factors. Here we study genetic isolation between populations of sculpins (Cottus) at 168 microsatellites. Genomic clines were fit using 480 individuals sampled across independent natural hybrid zones that have formed between one invading species and two separate populations of a resident species. Our analysis tests for deviations from neutral patterns of introgression at individual loci based on expectations given genome-wide admixture. Roughly 51% of the loci analysed displayed significant deviations. An overall deficit of interspecific heterozygotes in 26% and 21% of the loci suggests that widespread underdominance drives genomic isolation. At the same time, selection promotes introgression of almost 30% of the markers, which implies that hybridization may increase the fitness of admixed individuals. Cases of overdominance or epistatic interactions were relatively rare. Despite the similarity of the two hybrid zones in their overall genomic composition, patterns observed at individual loci show little correlation between zones and many fit different genotypic models of fitness. At this point, it remains difficult to determine whether these results are due to differences in external selection pressures or cryptic genetic differentiation of distinct parental populations. In the future, data from mapped genetic markers and on variation of ecological factors will provide additional insights into the contribution of these factors to variation in the evolutionary consequences of hybridization.

Introduction to “Ecological and Evolutionary Consequences after Invaders Hybridize”

The motivation for this special issue was a symposium organized by Ayres and Schierenbeck at the 2006 American Botanical Society annual meeting that took its title from Ellstrand and Schierenbeck’s highly cited 2000 paper in Proceedings of the National Academy of Science, ‘‘Hybridization as a Stimulus for the Evolution of Invasiveness’’. Ellstrand was the keynote speaker. As explored previously by Ellstrand and Schierenbeck (2000), the mixing of divergent genotypes can result in the creation of populations of hybrids that are more invasive than the parental species. The symposium sparked such interest in the participants and audience that Ellstrand suggested we collaborate on a special issue. Here we revisit the earlier examples (Schierenbeck and Ellstrand 2009), and in a series of papers, present case studies examining the ecological and evolutionary consequences of hybridization in plants which range from hybridization between cultivars in ornamental pears (Culley and Hardiman 2008), to introgressive hybridization between species (Gaskin and Kazmer 2008; Sloop et al. 2009), to the formation of diploid (Abbott et al. 2008) and allopolyploid hybrid species (Ainouche et al. 2008; Ayres et al. 2008). We also consider the interplay between sexual and clonal reproduction in invaders (Bailey et al. 2008) whether hybrid plants are by their nature more invasive than non-hybridized taxa in a meta-analysis (Whitney et al. 2008), and outline approaches to modeling hybrid population dynamics (Hall and Ayres 2008). The case studies should serve as cautionary tales against the casual introduction of nonnative taxa into areas occupied by conspecifics or congeners while this special issue illustrates the potential for hybrid studies to increase our understanding of evolution.

Review. Specificity in pollination and consequences for postmating reproductive isolation in deceptive Mediterranean orchids.

The type of reproductive isolation prevalent in the initial stages of species divergence can affect the nature and rate of emergence of additional reproductive barriers that subsequently strengthen isolation between species. Different groups of Mediterranean deceptive orchids are characterized by different levels of pollinator specificity. Whereas food-deceptive orchid species show weak pollinator specificity, the sexually deceptive Ophrys species display a more specialized pollination strategy. Comparative analyses reveal that orchids with high pollinator specificity mostly rely on premating reproductive barriers and have very little postmating isolation. In this group, a shift to a novel pollinator achieved by modifying the odour bouquet may represent the main isolation mechanism involved in speciation. By contrast, orchids with weak premating isolation, such as generalized food-deceptive orchids, show strong evidence for intrinsic postmating reproductive barriers, particularly for late-acting postzygotic barriers such as hybrid sterility. In such species, chromosomal differences may have played a key role in species isolation, although strong postmating-prezygotic isolation has also evolved in these orchids. Molecular analyses of hybrid zones indicate that the types and strength of reproductive barriers in deceptive orchids with contrasting premating isolation mechanisms directly affect the rate and evolutionary consequences of hybridization and the nature of species differentiation.

QTL ANALYSIS OF FLORAL TRAITS IN LOUISIANA IRIS HYBRIDS

The formation of hybrid zones between nascent species is a widespread phenomenon. The evolutionary consequences of hybridization are influenced by numerous factors, including the action of natural selection on quantitative trait variation. Here we examine how the genetic basis of floral traits of two species of Louisiana Irises affects the extent of quantitative trait variation in their hybrids. Quantitative trait locus (QTL) mapping was used to assess the size (magnitude) of phenotypic effects of individual QTL, the degree to which QTL for different floral traits are colocalized, and the occurrence of mixed QTL effects. These aspects of quantitative genetic variation would be expected to influence (1) the number of genetic steps (in terms of QTL substitutions) separating the parental species phenotypes; (2) trait correlations; and (3) the potential for transgressive segregation in hybrid populations. Results indicate that some Louisiana Iris floral trait QTL have large effects and QTL for different traits tend to colocalize. Transgressive variation was observed for six of nine traits, despite the fact that mixed QTL effects influence few traits. Overall, our QTL results imply that the genetic basis of floral morphology and color traits might facilitate the maintenance of phenotypic divergence between Iris fulva and Iris brevicaulis, although a great deal of phenotypic variation was observed among hybrids.

Evolutionary Dynamics of anIpomopsisHybrid Zone: Confronting Models with Lifetime Fitness Data

Interspecific hybridization is a recurring aspect of the evolution of many plant and animal groups. The temporal dynamics of hybrid zones and the evolutionary consequences of hybridization should depend on fitness of parental and hybrid individuals expressed in different environments. We measured lifetime fitness, including survival and reproduction, of plants of Ipomopsis aggregata, Ipomopsis tenuituba, and their F1 hybrids, in experimental plantings in a natural hybrid zone. Fitness, measured as the finite rate of increase ( lambda ), depended strongly on environment. Each parental species performed well in its home locale and poorly in the locale of the other species. Hybrids performed as well as parents overall but enjoyed their highest fitness in the hybrid site. Furthermore, F1 hybrids with I. tenuituba as maternal parent survived well only at the hybrid site, suggesting a cytonuclearxenvironment interaction. These results support an "environmental cline" model of hybrid zone dynamics, with complexities in the fitness of hybrids consistent also with an "evolutionary novelty" model. Combined with those of earlier studies of pollination, our results suggest that both vegetative adaptation to physical environment and floral adaptation to pollinators contribute to observed patterns of phenotypic expression in this hybrid zone and to persistence of the hybrid zone.

A secondary hybrid zone between diploid Dactylorhiza incarnata ssp. cruenta and allotetraploid D. lapponica (Orchidaceae)

Secondary hybrid zones are not uncommon in Dactylorhiza, but knowledge of ecological and evolutionary consequences of hybridization are scarce. Here, we assess interploidal gene flow and introgression in a hybrid zone between diploid Dactylorhiza incarnata ssp. cruenta (2n = 2x = 40) and its putative allotetraploid derivative D. lapponica (2n = 4x = 80). Photometric quantification of DNA content and morphology confirmed that triploids are abundant in sympatric populations in our study area. Allozyme segregation patterns in D. lapponica supported an allopolyploid origin, although unbalanced genotypes suggested rare pairings between homoeologous chromosomes. Photometric data and chromosome counts suggest backcrossing between the triploid hybrid and D. lapponica, and hence some hybrid fertility. Triploids are morphologically more similar to the tetraploids than the diploids, maybe owing to the hybrid origin of both triploids and tetraploids. The diploids and tetraploids were not more similar in the parapatric populations compared to when they occur in allopatry. This indicates that backcrossing rarely leads to introgression, or alternatively that allopatric populations are not isolated enough to prevent influx of pollen from the other species. Despite some evidence of backcrossing, our study gives few indications that widespread hybridization entails local breakdown of species boundaries. Rather, the hybrid zone may be a transient phenomenon due to intensive mowing, resulting in the opening of habitats and hence bringing the parental species into close contact.

Absence of Extensive Introgression between Xenopus gilli and Xenopus laevis laevis (Anura: Pipidae) in Southwestern Cape Province, South Africa

The evolutionary consequences of hybridization, including introgression, have been studied in many anuran amphibians (Lamb and Avise, 1986; Szymura and Barton, 1986), particularly in the African clawed frogs of the genus Xenopus (Tinsley, 1981; Kobel, 1996a; Picker et al., 1996). Species of Xenopus are found over much of sub-Saharan Africa and are mostly allopatric, though zones of sympatry and naturally occurring hybrids have been described (Picker, 1985; Tinsley et al., 1996; Yager, 1996). Although hybridization has been linked to allopolyploid speciation in Xenopus (Carr et al., 1987, Kobel, 1996b), the extent to which hybridization has facilitated genetic introgression among species has not been assessed.

Evolutionary and ecological consequences of interspecific hybridization in cladocerans

The evolutionary process of interspecific hybridization in cladocerans is reviewed based on ecological and population genetic data. The evolutionary consequences of hybridization, biogeographic patterns and fitness comparisons are analyzed within the conceptual framework of theories on hybridization. Among species of theD. longispina complex no interpopulational transition zones (hybrid zones) have been detected, but rather patchy distributions of hybrids and parentals have been found. Hybrids occur across broad geographic ranges and can be more abundant than parental species. Due to asexual reproduction (ameiotic parthenogenesis), hybrid breakdown can be avoided, and hybrids can even (temporarily) combine advantageous traits of both parental species. Evolutionary consequences may arise from repeated backcrossing, which in some cases results in introgression and patterns of reticulate evolution.