PHENOTYPIC AND GENETIC EFFECTS OF HYBRIDIZATION IN DARWIN'S FINCHES

Morphological consequences of hybridization were studied in a group of three interbreeding species of Darwin's finches on the small Galápagos island of Daphne Major in the inclusive years 1976 to 1992. Geospiza fortis bred with G. scandens and G. fuliginosa. Although interbreeding was always rare (< 5%), sufficient samples of measurements of hybrids and backcrosses were accumulated for analysis. Five beak and body dimensions and mass were measured, and from these two synthetic (principal-component) traits were constructed. All traits were heritable in two of the interbreeding species (G. fuliginosa were too rare to be analyzed) and in the combined samples of F, hybrids and backcrosses to G. fortis. In agreement with expectations from a model of polygenic inheritance, hybrid and backcross classes were generally phenotypically intermediate between the breeding groups that had produced them. Hybridization increased additive genetic and environmental variances, increased heritabilities to a moderate extent, and generally strengthened phenotypic and genetic correlations. New additive genetic variance introduced by hybridization is estimated to be two to three orders of magnitude greater than that introduced by mutation. Enhanced variation facilitates directional evolutionary change, subject to constraints arising from genetic correlations between characters. The Darwin's finch data suggest that these constraints become stronger when species with similar proportions hybridize, but some become weaker when the interbreeding species have different allometries. This latter effect of hybridization, together with an enhancement of genetic variation, facilitates evolutionary change in a new direction.     

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.     

Conspecific versus heterospecific gene exchange between populations of Darwin's finches

This study addresses the extent and consequences of gene exchange between populations of Darwin''s finches. Four species of ground finches (Geospiza) inhabit the small island of Daphne Major in the centre of the Galápagos archipelago. We undertook a study of microsatellite DNA variation at 16 loci in order to quantify gene flow within species owing to immigration and between species owing to hybridization. A combination of pedigrees of observed breeders and assignments of individuals to populations by the program Structure enabled us to determine the frequency of gene exchange and the island of origin of immigrants in some cases. The relatively large populations of Geospiza fortis and G. scandens receive conspecific immigrants at a rate of less than one per generation. They exchange genes more frequently by rare but repeated hybridization. Effects of heterospecific gene flow from hybridization are not counteracted by lower fitness of the offspring. As a result, the standing genetic variation of the two main resident populations on Daphne Major is enhanced to a greater extent by introgressive hybridization than through breeding with conspecific immigrants. Immigrant G. fuliginosa also breeds with G. fortis. Conspecific immigration was highest in the fourth species, G. magnirostris. This species is much larger than the other three and perhaps for this reason it has not bred with any of them. The source island of most immigrants is probably the neighbouring island of Santa Cruz. Evolutionary change may be inhibited in G. magnirostris by continuing gene flow, but enhanced in G. fortis and G. scandens by introgressive hybridization.     

NATURAL SELECTION ON BEAK AND BODY SIZE IN THE SONG SPARROW

We documented temporal patterns of natural selection on beak and body traits in a song sparrow population. We looked for evidence of selection in association with reproduction and overwinter survival in order to identify the conditions under which size in beak and body traits is adaptive. We also attempted to identify the specific traits most closely associated with fitness under these conditions. Selection was observed in association with both survival and reproduction. Patterns of selection differed between the sexes. Selection on males was weak and stabilizing in association with overwinter survival. Selection on females was strong, was both stabilizing and directional, and was associated with both survival and reproduction. In females, traits that enhanced juvenile survival also reduced reproductive success; i.e., there was a trade-off between survival and reproduction. Patterns of selection in the song sparrow parallel those reported for the Galápagos finch, Geospiza fortis. However, in song sparrows, selection occurred mainly on tarsus length and beak length, and not on beak depth or width as in G. fortis. This difference may occur because most North American sparrows partition food resources by habitat, while most Galápagos ground finches partition food by seed size.     

CULTURAL INHERITANCE OF SONG AND ITS ROLE IN THE EVOLUTION OF DARWIN'S FINCHES

Songs of Darwin's finches were studied on the Galápagos Island of Daphne Major from 1976 to 1995. A single, structurally simple, and unvarying song is sung throughout life by each male of the two common species, Geospiza fortis (medium ground finch) and G. scandens (cactus finch). Songs of the two species differ strongly in quantitative features, and individual variation among males is much broader in G. fortis than in G. scandens. Although there are exceptions, songs of sons strongly resemble the songs of their fathers. They also resemble the songs of their paternal grandfathers, but not their maternal grandfathers, indicating that they are culturally inherited and not genetically inherited. Female G. fortis display a tendency to avoid mating with males that sing the same type of song as their father. They also avoid mating with males that sing heterospecific song, with very rare exceptions. Thus song, an evolving, culturally inherited trait, is an important factor in species recognition and mate choice. It constrains the mating of females to conspecifics, even when there is no genetic penalty to interbreeding, and thus may play a crucial role in species formation by promoting genetic isolation on secondary contact. The barrier is leaky in that occasional errors in song transmission result in misimprinting, which leads to a low incidence of hybridization and introgression. Introgression slows the rate of postzygotic isolation, but can produce individuals in novel genetic and morphological space that can provide the starting point of a new evolutionary trajectory.     

Population Variation in Continuously Varying Traits as an Ecological Genetics Problem

The niche variation hypothesis is an adaptive explanation forvariation within populations and for, the differences in variationbetween populations in morphological, physiological or behavioraltraits. It has received only partial support from empiricaltests and has been criticized on theoretical grounds. Recentquantitative genetic models have made an advance by exploringthe effects of mutation, migration, mating pattern and selectionon phenotypic variance. These models are reviewed and theirmost important features are integrated in a new model. In thismodel population variation is in a state of balance betweenthe opposing forces of mutation and immigration, which tendto elevate variation, and selection and possibly genetic drifttending to decrease it. Populations exhibiting different levelsof variation are interpereted as having different equilibriumpoints, and it is the task of empirical studies to determinethe relative magnitudes of the opposing factors. An exampleis given from studies of Darwin's finches. Geospiza fortis variesmore than G. scandens on Isla Daphne Major, Galápagos,in several morphological traits including beak and body size.This is explained, assuming equal mutation rates in the twospecies, as the result of more frequent genetic input to theG. fortis population, through occasional hybridization withimmigrant G. fuliginosa, and relaxed stabilizing selection.Stabilizing selection is less intense on G.fortis than on G.scandens because the G. fortis population has a broader niche;there is both a within-phenotype and betweenphenotype componentto the broad niche of G. fortis. The success of theory in explainingpopulation variation is discussed, and it is concluded thatempirical studies lag far behind theory.     

Evolution of postzygotic reproductive isolation in galliform birds: analysis of first and second hybrid generations and backcrosses

The process of speciation is a crucial aspect of evolutionary biology. In this study, we analysed the patterns of evolution of postzygotic reproductive isolation in Galliformes using information on hybridization and genetic distance among species. Four main patterns arose: (1) hybrid inviability and sterility in F₁ hybrids increase as species diverge; (2) the presence of geographical overlap does not affect the evolution of postzygotic isolation; (3) the galliforms follow Haldane's rule; (4) hybrid inviability is higher in F₂ than in F₁ hybrids, but does not appear to be increased in the backcrosses. This study contributes to the growing evidence suggesting that the patterns of evolution of postzygotic isolation and the process of speciation are shared among avian groups (and animals in general). In particular, our results support the notion of F₂ hybrid inviability as being key for the maintenance of species genetic integrity when prezygotic isolation barriers are overcome in closely related species, in which postzygotic isolation in the F₁ hybrid might still not be fully developed. To the contrary, hybrids from backcrosses did not show serious inviability problems (at least not more than F₁ hybrids), demonstrating that they could generate gene flow among bird species. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 528–542.     

REPRODUCTIVE ISOLATION AND INTROGRESSION BETWEEN NOTROPIS CORNUTUS AND NOTROPIS CHRYSOCEPHALUS (FAMILY CYPRINIDAE): COMPARISON OF MORPHOLOGY,ALLOZYMES, AND MITOCHONDRIAL DNA

Hybrid zones in fluvial fishes may be heterogeneous from drainage to drainage. The comparison of data from morphology, allozymes, and mitochondrial DNA (mtDNA) indicates variability in the causes and degree of restriction of gene flow between Notropis cornutus and Notropis chrysocephalus. Allozyme marker loci show frequency-dependent introgression; i.e., the rarer species, whichever it is at a particular locality, tends to exhibit a higher proportion of introgressed alleles. Unlike allozymes, introgression of mtDNA haplotypes varies geographically. In westward-flowing Michigan drainages, N. cornutus mtDNA haplotypes are more common in F₁ hybrids and backcrosses, independent of parental frequencies. In eastward-flowing Michigan drainages, N. chrysocephalus mtDNA is more common in F₁ hybrids and backcrosses; this pattern may be due to local ecological effects or frequency-dependent introgression. Morphological data alone are not sufficient to distinguish all classes of hybrids. The lack of concordance of morphological, allozymic, and mtDNA introgression patterns implies operation of one or two factors: 1) geographically variable patterns of selection against different hybrid and backcross combinations or 2) genetic differences between Michigan populations inhabiting eastward- and westward-flowing drainage systems accumulated during historical isolation.     

Body condition (Wr) and reproductive potential of bighead and silver carp hybrids: Postzygotic selection in the Mississippi River Basin

Invasive bighead (Hypophthalmichthys nobilis) and silver carp (H. molitrix) are reproductively isolated in their native range, but form a bimodal, multigenerational hybrid swarm within the Mississippi River Basin (MRB). Despite observed F₁ hybrid superiority in experimental settings, effects of postzygotic selection on bighead and silver carp hybrids have not been tested in a natural system. Individual parent and hybrid genotypes were resolved at 57 species‐specific loci and used to evaluate postzygotic selection for body condition (W_r) and female reproductive potential (presence of spawning stage gonads and gonadosomatic index [GSI]) in the MRB during 2009–2011. Body condition in the Marseilles Reach, Illinois River declined with a decrease in species‐specific allele frequency from 1.0 to 0.4 for each species and early generation hybrids (F₁, F₂, and first‐generation backcross) had lower mean W_r than late generation hybrids (2nd+ generation backcrosses) and parentals. Proportions of stage IV and stage V (spawning stage) female gonads differed between bighead and silver carp, but not among parentals and their early and late generation hybrids within the MRB. Mean GSI values did not differ between parentals and hybrids. Because reproductive potential did not differ between hybrids and parentals, our results suggest that early generation hybrids occur in low frequency either as a factor of poor condition (W_r) and postreproductive survival, infrequent reproductive encounters by parental bighead and silver carp, or selection pressures acting on juvenile or immature life stages. Our results suggest that a combination of genetic and environmental factors may contribute to the postzygotic success of bighead and silver carp hybrids in the Mississippi River Basin.     

Divergence with gene flow as facilitated by ecological differences: within-island variation in Darwin's finches

Divergence and speciation can sometimes proceed in the face of, and even be enhanced by, ongoing gene flow. We here study divergence with gene flow in Darwin''s finches, focusing on the role of ecological/adaptive differences in maintaining/promoting divergence and reproductive isolation. To this end, we survey allelic variation at 10 microsatellite loci for 989 medium ground finches (Geospiza fortis) on Santa Cruz Island, Galápagos. We find only small genetic differences among G. fortis from different sites. We instead find noteworthy genetic differences associated with beak. Moreover, G. fortis at the site with the greatest divergence in beak size also showed the greatest divergence at neutral markers; i.e. the lowest gene flow. Finally, morphological and genetic differentiation between the G. fortis beak-size morphs was intermediate to that between G. fortis and its smaller (Geospiza fuliginosa) and larger (Geospiza magnirostris) congeners. We conclude that ecological differences associated with beak size (i.e. foraging) influence patterns of gene flow within G. fortis on a single island, providing additional support for ecological speciation in the face of gene flow. Patterns of genetic similarity within and between species also suggest that interspecific hybridization might contribute to the formation of beak-size morphs within G. fortis.     

Genetic structure of a hybrid zone between two violets,Viola rossii Hemsl. and V. bissetii Maxim.: dominance of F1 individuals in a narrow contact range

The genetic composition of a hybrid zone can provide insight into the evolution of diversification in plants. We carried out morphological and amplified fragment length polymorphism analyses to investigate the genetic composition of a hybrid zone between two violets, Viola bissetii Hemsl. and Viola rossii Maxim. Our aim was to clarify the formation and maintenance of hybrids between these Viola species. We found that most hybrid individuals (V. bissetii × V. rossii) were of the F₁ generation, with a few of the F₂ generation. We found no backcrosses. The scarcity of post‐F₁ hybrids indicates that a species barrier is established between the parental species. The F₁‐dominated hybrid zone occupied only a narrow, intermediate ecotone between the parental habitats, suggesting that selection by environmental factors against hybrids may help to maintain the current conditions in this hybrid zone.     

Variation in contact zone dynamics between two species of topminnows, Fundulus notatus and F. olivaceus, across isolated drainage systems

Spatially variable selection pressure within heterogeneous environments can result in the evolution of specialist phenotypes that facilitate co-occurrence of closely related species and limit genetic exchange. If divergent selection pressures maintain reproductive isolation, hybridization is expected to correlate with the strength of underlying ecological gradients and the traits shaped by adaptive processes. We sampled ten replicate topminnow (Fundulus olivaceus and Fundulus notatus) hybrid zones in isolated drainages throughout central and southern North America. In all drainages, species were distributed in an upstream–downstream manner with contact zones localized at confluences featuring abrupt shifts from tributary to river habitat. In two drainages, the typical up and downstream positions of species were reversed. Phenotype differences between the species reflect predicted selection differences along stream gradients. Downstream populations (lower food availability and greater predator pressure) generally showed larger investment in reproduction (higher gonadal somatic index), smaller body size and lower somatic condition compared to upstream populations. Phenotypic differences between the species in the two reversed drainages were consistent with convergence of life history traits in the respective habitats. Phenotypes of individuals of hybrid origin (F₁ hybrids or backcrosses) were not significantly different from the average of the two parental forms, though there were trends towards reduced fitness. The prevalence of hybridization among drainages ranged from no hybrids in two drainages to near random mating. The strongest correlates of hybridization rate among replicate hybrid zones were similarity in body shape and the homogeneity of habitat through tributary-river confluences. The two reversed orientation hybrid zones also exhibited high prevalence of hybrids suggesting that phenotypic convergence could lead to increased hybridization.     

SEX CHROMOSOME LINKAGE OF MATE PREFERENCE AND COLOR SIGNAL MAINTAINS ASSORTATIVE MATING BETWEEN INTERBREEDING FINCH MORPHS

Assortative mating is a key aspect in the speciation process because it is important for both initial divergence and maintenance of distinct species. However, it remains a challenge to explain how assortative mating evolves when diverging populations are undergoing gene flow (e.g., during hybridization). Here I experimentally test how assortative mating is maintained with frequent gene flow between diverged head‐color morphs of the Gouldian finch (Erythrura gouldiae). Contrary to the predominant view on the development of sexual preferences in birds, cross‐fostered offspring did not imprint on the phenotype of their conspecific (red or black morphs) or heterospecific (Bengalese finch) foster parents. Instead, the mating preferences of F₁ and F₂ intermorph‐hybrids are consistent with inheritance on the Z chromosomes, which are also the location for genes controlling color expression and the genes causing low fitness of intermorph‐hybrids. Genetic associations between color signal and preference loci on the sex chromosomes may prevent recombination from breaking down these associations when the morphs interbreed, helping to maintain assortative mating in the face of gene flow. Although sex linkage of reproductively isolating traits is theoretically expected to promote speciation, social and ecological constraints may enforce frequent interbreeding between the morphs, thus preventing complete reproductive isolation.     

Interspecific hybridization between common and tepary beans: increased hybrid embryo growth,fertility, and efficiency of hybridization through recurrent and congruity backcrossing

Cultivated common bean (Phaseolus vulgaris L.) and tepary bean (Phaseolus acutifolius A. Gray) genotypes possessing desirable agronomic traits were hybridized. The F₁ hybrids were backcrossed twice with the common bean (i.e., recurrent backcrossing). Also, alternate backcrosses with common and tepary beans (i.e., congruity backcrossing) were carried out. Embryo culture was necessary for all initial interspecific crosses, and its requirement was proportionally lower when the common bean was used as the recurrent parent and as the last parent of congruity backcrosses. Modification of the embryo culture technique was necessary to produce congruity hybrids. Effects of both tepary and common bean genotypes on the success rate of hybridization were observed. Tepary accession G 40001 and common bean cultivar ICA Pijao facilitated interspecies hybridization. Growth of hybrid embryos before rescue, recovery of mature hybrid plants, and the vigor and fertility of F₁ hybrids all increased with increased recurrent and congruity backcrosses and intermatings between male-sterile F₁ and selected fertile F₂ plants of the third and fifth congruity backcrosses. Introgression of tepary genes was verified by means of seed protein electrophoretic analysis and morphological markers. The results suggest that congruity backcrossing can help to gradually reduce or overcome P. vulgaris x P. acutifolius hybridization barriers such as genotype incompatibility, early embryo abortion, hybrid sterility, and lower frequencies of hybridization.     

THE RELATIONSHIPS BETWEEN MALE AND FEMALE FERTILITY AND AMONG TAXA IN DIPLOID WHEATS

Pollen stainability appears to be a reliable indication of the ultimate seed set in diploid interspecific hybrid and backcross populations in Triticum L. The correlation between percent pollen stained and number of seeds set is positive and highly significant (r = 0.92). Estimates of male and female fertility in the hybrids and backcrosses are interpreted to indicate that the domesticated diploid Triticum monococcum L. and wild diploid T. boeoticum Boiss. em. Schiem, are one and the same species, and that T. urartu Tum. is not a variety of monococcum or boeoticum, but rather a separate species. The F₁ hybrids and backcrosses between monococcum and boeoticum are normally male and female fertile. The F₁ hybrids between monococcum and urartu are completely sterile and complete to partial sterility exists in backcrosses.     

Population variation and hybridization: Comparison of finches from two archipelagos

Summary Some populations of Darwin's Finches (Emberizinae) are exceptionally variable in body size and beak traits as a result of introgressive hybridization. A study of museum specimens of honeycreeper-finches (Carduelinae) from the Hawaiian islands was undertaken to see if the same phenomenon was manifested by a different phyletic group of finches in a different archipelago. Five hundred and twenty-four specimens of the seven species with finch-like bills were measured and their coefficients of variation were compared with those of the ground finch group (six species) of Darwin's Finches. Coefficients were smaller in the Hawaiian finches. Sympatric and, hence, potentially hybridizing species on the island of Hawaii were not consistently more variable than the allopatric species on other islands in the archipelago. The one species with both sympatric and allopatric populations did not show greater variation in the sympatric population. There is little evidence from these comparisons of hybridization occurring in the last 100 years. The difference between the two finch faunas can be explained in terms of two factors. Finches have been present for a longer time in the Hawaiian archipelago than in the Galápagos archipelago and have had more time to not only diversify but to evolve pre- and post-zygotic isolating mechanisms. In the generally less seasonal and floristically richer Hawaiian islands they have evolved greater dietary specializations. Beak traits adapted to specialist feeding may have been under stronger stabilizing selection and hybrids (if formed) may have been at a strong disadvantage in the absence of an ecological niche intermediate between the niches of the two parental species. Results of published electrophoretic studies of genetic variation suggest that the early phase of differentiation, involving occasional introgressive hybridization, may last for up to 5 million years.     

ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT-DEPENDENT HYBRID FITNESS

“Ecological” speciation occurs when reproductive isolation evolves as a consequence of divergent selection between populations exploiting different resources or environments. We tested this hypothesis of speciation in a young stickleback species pair by measuring the direct contribution of ecological selection pressures to hybrid fitness. The two species (limnetic and benthic) are strongly differentiated morphologically and ecologically, whereas hybrids are intermediate. Fitness of hybrids is high in the laboratory, especially F₁ and F₂ hybrids (backcrosses may show some breakdown). We transplanted F₁ hybrids to enclosures in the two main habitats in the wild to test whether the distribution of resources available in the environment generates a hybrid disadvantage not detectable in the laboratory. Hybrids grew more slowly than limnetics in the open water habitat and more slowly than benthics in the littoral zone. Growth of F₁ hybrids was inferior to the average of the parent species across both habitats, albeit not significantly. The contrast between laboratory and field results supports the hypothesis that mechanisms of F₁ hybrid fitness in the wild are primarily ecological and do not result from intrinsic genetic incompatibilities. Direct selection on hybrids contributes to the maintenance of sympatric stickleback species and may have played an important role in their origin.     

Postzygotic isolation drives genomic speciation between highly cryptic Hypocnemis antbirds from Amazonia

How species evolve reproductive isolation in the species-rich Amazon basin is poorly understood in vertebrates. Here, we sequenced a reference genome and used a genome-wide sample of SNPs to analyze a hybrid zone between two highly cryptic species of Hypocnemis warbling-antbirds—the Rondonia warbling-antbird (H. ochrogyna) and Spix's warbling-antbird (H. striata)—in a headwater region of southern Amazonia. We found that both species commonly hybridize, producing F₁s and a variety of backcrosses with each species but we detected only one F₂-like hybrid. Patterns of heterozygosity, hybrid index, and interchromosomal linkage disequilibrium in hybrid populations closely match expectations under strong postzygotic isolation. Hybrid zone width (15.4 km) was much narrower than expected (211 km) indicating strong selection against hybrids. A remarkably high degree of concordance in cline centers and widths across loci, and a lack of reduced interspecific F_st between populations close to versus far from the contact zone, suggest that genetic incompatibilities have rendered most of the genome immune to introgression. These results support intrinsic postzygotic isolation as a driver of speciation in a moderately young cryptic species pair from the Amazon and suggest that species richness of the Amazon may be grossly underestimated.     

Early generation hybrids may drive range expansion of two invasive fishes

1. Introgressive hybridisation between two invasive species has the potential to contribute to their invasion success and provide genetic resiliency to rapidly adapt to new environments. Additionally, differences in the behaviour of hybrids may lead to deleterious ecosystem effects that compound any negative impacts of the invading parental species.
2. Invasive silver carp (Hypophthalmichthys molitrix) and bighead carp (Hypophthalmichthys nobilis) provide an opportunity to evaluate how hybridisation may influence the behaviour, dispersal, and spread of an invasive species introgressive complex. In order to investigate the role hybrids may have in the invasion ecology of bigheaded carps, we examined the distribution, movements, and environmental cues for movement of two invasive fishes and their hybrids in the Illinois River (U.S.A.).
3. Early generation hybrids (e.g. F₁,F₂, and first-generation backcross individuals) composed a greater proportion of the population at the invasion front where abundances of bigheaded carp were low. A greater proportion of early hybrids passed through dams upstream towards the invasion front than did other hybrids and parental species.
4. The movements and environmental cues for movement of late-generation backcrosses (more genetically similar to parental genotype) were not different from the parental species with which they shared the most alleles. Although the direction of the relationship between movement and environment was sometimes different for the parental species and associated advanced generation hybrids, these results indicate that management for parental species will also affect most hybrids.
5. Although early generation hybrids are rare, our results indicate they may disperse towards low-density population zones (i.e. invasion fronts) or are produced at greater frequency in low-density areas. These rare hybrids have the potential to produce a variety of unique genetic combinations that could result in more rapid adaptation of a non-native population to their invaded range potentially facilitating the establishment of invasive species.