Primary Intergradation Research Articles

Historical allopatry and secondary contact or primary intergradation in the Puerto Rican crested anole, Anolis cristatellus, on Vieques Island in the Caribbean

AbstractRecent work has revealed surprisingly deep mitochondrial genetic divergence in the lizard Anolis cristatellus among samples obtained from the small Caribbean island of Vieques. Here we sought to determine whether this had resulted from natural or anthropogenic causes, and (if the former) whether divergence occurred in a biogeographical context of allopatry followed by secondary contact, or via isolation-by-distance across the species’ historical range. We first estimated a mitochondrial gene tree for 379 samples and then genotyped 3407 single nucleotide polymorphic sites from 48 individuals using a modified genotyping-by-sequencing approach. We found that A. cristatellus samples from Vieques belong to two highly divergent mitochondrial subclades, but the geographical distribution of these haplogroups indicates that this pattern is probably natural in origin. Analysis of our single nucleotide polymorphic dataset revealed differentiation that is consistent with isolation-by-distance between the western and eastern ends of Vieques, suggesting that the overall pattern of divergence probably reflects primary intergradation with a mitochondrial break on the historical Puerto Rico Bank palaeo-island that happened to coincide with the present-day location of Vieques. Our findings help to underline the growing consensus that results from a single genetic marker can prove highly misleading in studies of historical population genetic structure.

Plant speciation across environmental gradients and the occurrence and nature of hybrid zones

AbstractEnvironmental gradients are very common and many plant species respond to them through adaptive genetic change. This can be a first step along a continuum of change that leads ultimately to the origin of fully reproductively isolated forms, i.e., ‘biological species’. Before complete reproductive isolation is achieved, hybrid zones may form between divergent lineages either through primary intergradation or secondary contact. Here, I review the literature on plant hybrid zones between native species and highlight: mode of origin (primary intergradation versus secondary contact); distribution among plant families, genera and life form; type and genotypic composition related to strength and type of reproductive isolation between parental lineages; nature of prezygotic and postzygotic reproductive barriers; level and direction of gene flow; and the stability of hybrid zones in the face of climate change. The total number of plant hybrid zones detected in a literature search was surprisingly small (137). This was the case even for areas of the world with a long history of research into plant evolution, ecology and systematics. Reasons for this are discussed, including the possibility that plant hybrid zones are naturally rare in the wild. Only for a few hybrid zones have attempts been made to distinguish between formation by primary intergradation or secondary contact, and it is assumed that most hybrid zones originate through secondary contact. From the limited information available, it appears that plant hybrid zones may frequently move in response to climate change, but long‐term studies are required to confirm this.

Heterogeneous genome divergence, differential introgression, and the origin and structure of hybrid zones.

Hybrid zones have been promoted as windows on the evolutionary process and as laboratories for studying divergence and speciation. Patterns of divergence between hybridizing species can now be characterized on a genomewide scale, and recent genome scans have focused on the presence of 'islands' of divergence. Patterns of heterogeneous genomic divergence may reflect differential introgression following secondary contact and provide insights into which genome regions contribute to local adaptation, hybrid unfitness and positive assortative mating. However, heterogeneous genome divergence can also arise in the absence of any gene flow, as a result of variation in selection and recombination across the genome. We suggest that to understand hybrid zone origins and dynamics, it is essential to distinguish between genome regions that are divergent between pure parental populations and regions that show restricted introgression where these populations interact in hybrid zones. The latter, more so than the former, reveal the likely genetic architecture of reproductive isolation. Mosaic hybrid zones, because of their complex structure and multiple contacts, are particularly good subjects for distinguishing primary intergradation from secondary contact. Comparisons among independent hybrid zones or transects that involve the 'same' species pair can also help to distinguish between divergence with gene flow and secondary contact. However, data from replicate hybrid zones or replicate transects do not reveal consistent patterns; in a few cases, patterns of introgression are similar across independent transects, but for many taxa, there is distinct lack of concordance, presumably due to variation in environmental context and/or variation in the genetics of the interacting populations.

Variability and status of intraspecific forms of sand sculpin Leocottus kesslerii (Cottidae)

Results of study of phenotypic variation of sand sculpin Leocottus kesslerii in Lake Baikal and water bodies of the Baikal region are presented. It was found that interpopulation variation of characters has a gradient pattern, while differences reach taxonomically significant level only between samples with maximum and minimal values of characters. Since variation of characters is characterized by primary intergradation and isolation barriers within the range are not insurmountable, it seems inexpedient to assign an independent taxonomic status to any forms either in proper Baikal or beyond its limits. Sand sculpin is a monotypic polymorphic species, whose phenotypic isolation of populations reflects the level of their spatial and ecological segregation.

Revisiting the Iberian honey bee (Apis mellifera iberiensis) contact zone: maternal and genome-wide nuclear variations provide support for secondary contact from historical refugia.

Dissecting diversity patterns of organisms endemic to Iberia has been truly challenging for a variety of taxa, and the Iberian honey bee is no exception. Surveys of genetic variation in the Iberian honey bee are among the most extensive for any honey bee subspecies. From these, differential and complex patterns of diversity have emerged, which have yet to be fully resolved. Here, we used a genome-wide data set of 309 neutrally tested single nucleotide polymorphisms (SNPs), scattered across the 16 honey bee chromosomes, which were genotyped in 711 haploid males. These SNPs were analysed along with an intergenic locus of the mtDNA, to reveal historical patterns of population structure across the entire range of the Iberian honey bee. Overall, patterns of population structure inferred from nuclear loci by multiple clustering approaches and geographic cline analysis were consistent with two major clusters forming a well-defined cline that bisects Iberia along a northeastern-southwestern axis, a pattern that remarkably parallels that of the mtDNA. While a mechanism of primary intergradation or isolation by distance could explain the observed clinal variation, our results are more consistent with an alternative model of secondary contact between divergent populations previously isolated in glacial refugia, as proposed for a growing list of other Iberian taxa. Despite current intense honey bee management, human-mediated processes have seemingly played a minor role in shaping Iberian honey bee genetic structure. This study highlights the complexity of the Iberian honey bee patterns and reinforces the importance of Iberia as a reservoir of Apis mellifera diversity.

Phylogeography of speciation: allopatric divergence and secondary contact between outcrossing and selfingClarkia

AbstractThe origins of hybrid zones between parapatric taxa have been of particular interest for understanding the evolution of reproductive isolation and the geographic context of species divergence. One challenge has been to distinguish between allopatric divergence (followed by secondary contact) versus primary intergradation (parapatric speciation) as alternative divergence histories. Here, we use complementary phylogeographic and population genetic analyses to investigate the recent divergence of two subspecies ofClarkia xantianaand the formation of a hybrid zone within the narrow region of sympatry. We tested alternative phylogeographic models of divergence using approximate Bayesian computation (ABC) and found strong support for a secondary contact model and little support for a model allowing for gene flow throughout the divergence process (i.e. primary intergradation). Two independent methods for inferring the ancestral geography of each subspecies, one based on probabilistic character state reconstructions and the other on palaeo‐distribution modelling, also support a model of divergence in allopatry and range expansion leading to secondary contact. The membership of individuals to genetic clusters suggests geographic substructure within each taxon where allopatric and sympatric samples are primarily found in separate clusters. We also observed coincidence and concordance of genetic clines across three types of molecular markers, which suggests that there is a strong barrier to gene flow. Taken together, our results provide evidence for allopatric divergence followed by range expansion leading to secondary contact. The location of refugial populations and the directionality of range expansion are consistent with expectations based on climate change since the last glacial maximum. Our approach also illustrates the utility of combining phylogeographic hypothesis testing with species distribution modelling and fine‐scale population genetic analyses for inferring the geography of the divergence process.

Spatio-temporal variation in the structure of a chromosomal polymorphism zone in the house mouse

Several long-term temporal analyses of the structure of Robertsonian (Rb) hybrid zones in the western house mouse, Mus musculus domesticus, have been performed. Nevertheless, the detection of gradual or very rapid variations in a zone may be overlooked when the time elapsed between periods of study is too long. The Barcelona chromosomal polymorphism zone of the house mouse covers about 5000, km(2) around the city of Barcelona and is surrounded by 40 chromosome telocentric populations. Seven different metacentrics and mice with diploid numbers between 27 and 40 chromosomes and several fusions in heterozygous state (from one to seven) have been reported. We compare the present (period 2008-2010) and past (period 1996-2000) structure of this zone before examining its dynamics in more detail. Results indicate that there is not a Rb race in this area, which is consistent with the proposal that this zone was probably originated in situ, under a primary intergradation scenario. The lack of individuals with more than five metacentrics in heterozygous state in the current period suggests that selection acted against such mice. By contrast, this situation did not occur for mice with fewer than five fusions in heterozygous condition. Changes in human activity may affect the dynamics of gene flow between subpopulations, thus altering the chromosomal composition of certain sites. Although these local variations may have modified the clinal trend for certain metacentrics, the general staggered structure of the zone has not varied significantly in a decade.

Morphological variation in house mice from the Robertsonian polymorphism area of Barcelona

Morphometric variation in the Robertsonian polymorphism zone of Barcelona of Mus musculus domesticus was studied by geometric morphometrics. This system is characterized by populations of reduced diploid number (2n = 27–39) surrounded by standard populations (2n = 40). We investigated the morphological variation in mice from this area, as well as the effect of geographical distance and karyotype on this variation. We also investigated the degree of co-variation between the two functional units of the mandible to explore the origin of this system (primary intergradation or secondary contact). The size and shape of the cranium, mandible and scapula were analysed for 226 specimens grouped by population, chromosome number and structural heterozygosity. Size was estimated as the centroid size, and shape was estimated after Procrustes superimposition. No significant differences in size between populations or chromosomal groups were detected. Diploid number, structural heterozygosity and local geographical isolation contributed to the differentiation in shape. Morphological differentiation between standard mice and Robertsonian specimens was observed, suggesting genetic isolation between these groups. Co-variation between the ascending ramus and alveolar region of the mandible was quantified by the trace correlation between landmark subsets of these modules. The trace values showed an ascending trend, correlated with the distance from the centre of the polymorphism area, a pattern consistent with a primary intergradation scenario. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 97, 555–570.

Population structure of a lodgepole pine (Pinus contorta) and jack pine (P. banksiana) complex as revealed by random amplified polymorphic DNA.

We studied the population structure of a lodgepole (Pinus contorta Dougl.) and jack pine (Pinus banksiana Lamb.) complex in west central Alberta and neighboring areas by assessing random amplified polymorphic DNA (RAPD) variability in 23 lodgepole pine, 9 jack pine, and 8 putative hybrid populations. Of 200 random primers screened, 10 that amplified 39 sharp and reproducible RAPDs were chosen for the study. None of the 39 RAPDs were unique to the parental species. RAPD diversity ranged from 0.085 to 0.190 among populations and averaged 0.143 for lodgepole pine, 0.156 for jack pine, 0.152 for hybrids, and 0.148 for all 40 populations. The estimated population differentiation based on G(ST) was 0.168 for hybrids, 0.162 for lodgepole pine, 0.155 for jack pine, and 0.247 across all 40 populations. Cluster analysis of genetic distances generally separated jack pine from lodgepole pine and hybrids, but no division could be identified that further separated lodgepole pine from hybrids. The observed weak to mild trend of "introgression by distance" in the complex and neighbouring areas was consistent with the view that introgressive hybridization between lodgepole and jack pines within and outside the hybrid zone may have been through secondary contact and primary intergradation, respectively.

Spatial models for hybrid zones.

We introduce a spatially explicit model of natural hybrid zones that allows us to consider how patterns of allele frequencies and linkage disequilibria change over time. We examine the influence of hybrid zone origins on patterns of variation at two loci, a locus under selection in a two-patch environment, and a linked neutral locus. We consider several possible starting conditions that represent explicit realizations of two alternative scenarios for hybrid zone origins: primary intergradation and secondary contact. Our results indicate that in some circumstances, differences in hybrid zone origins will result in substantially different patterns of variation that may persist for thousands of generations. Our conclusions are generally similar to those previously derived from partial differential equations, but there are also some important differences.

Inferences about the origin of a field cricket hybrid zone from a mitochondrial DNA phylogeny.

Two closely related eastern North American field crickets, Gryllus firmus and G. pennsylvanicus, hybridize along a zone that extends from Connecticut and the Hudson River Valley, south along the eastern front of the Appalachian Mountains to at least Virginia. Here we use mitochondrial DNA (mtDNA) sequences to construct a population phylogeny for this pair of hybridizing cricket species. Using a phylogenetic approach, we attempt to discriminate between alternative population histories (secondary contact vs. primary intergradation) leading to formation of the hybrid zone. A strict consensus tree, based on > 1600 bp of the COI-COII region of the mtDNA genome, reveals four exclusive groups, which correspond to regional grouping of conspecific crickets. Surprisingly, the mtDNA sequence data do not reveal any synapomorphies for either G. pennsylvanicus or G. firmus. However, the mtDNA data do reveal a clear north-south split within each of the cricket species, a pattern not seen for morphological or other molecular characters. The biogeographical history of the north-south divergence events remains a puzzle. Observed gene genealogies support a model of secondary contact for the southern part of the hybrid zone. Sequence divergence data argue that lineages currently found in New York and New England were already distinct when this region became habitable following the most recent glaciation.

Incipient species formation in salamanders of the Ensatina complex.

The Ensatina eschscholtzii complex of plethodontid salamanders, a well-known "ring species," is thought to illustrate stages in the speciation process. Early research, based on morphology and coloration, has been extended by the incorporation of studies of protein variation and mitochondrial DNA sequences. The new data show that the complex includes a number of geographically and genetically distinct components that are at or near the species level. The complex is old and apparently has undergone instances of range contraction, isolation, differentiation, and then expansion and secondary contact. While the hypothesis that speciation is retarded by gene flow around the ring is not supported by molecular data, the general biogeographical hypothesis is supported. There is evidence of a north to south range expansion along two axes, with secondary contact and completion of the ring in southern California. Current research targets regions once thought to show primary intergradation, but which molecular markers reveal to be zones of secondary contact. Here emphasis is on the subspecies E. e. xanthoptica, which is involved in four distinct secondary contacts in central California. There is evidence of renewed genetic interactions upon recontact, with greater genetic differentiation within xanthoptica than between it and some of the interacting populations. The complex presents a full array of intermediate conditions between well-marked species and geographically variable populations. Geographically differentiated segments represent a diversity of depths of time of isolation and admixture, reflecting the complicated geomorphological history of California. Ensatina illustrates the continuing difficulty in making taxonomic assignments in complexes studied during species formation.

Species‐independent, geographical structuring of chloroplast DNA haplotypes in a montane herb Ipomopsis (Polemoniaceae)

Two hypotheses have been proposed to explain the occurrence of hybrid zones between red‐flowered Ipomopsis aggregata and white‐flowered I. tenuituba. Either local adaptation to hummingbird and hawkmoth pollinators has given rise to sympatric (or parapatric) divergence of flower colour and morphology (primary intergradation at hybrid zones), or alternatively two previously allopatric species are coming into contact at several geographical areas of secondary intergradation. We examined restriction site patterns in nuclear DNA (nrDNA), chloroplast DNA (cpDNA) and mitochondrial DNA (mtDNA) from populations of I. aggregata and I. tenuituba representing seven zones of sympatry. No variation was detected in a 350‐bp fragment of mtDNA and uninformative levels of variation were observed for nrDNA. We detected 22 potentially informative restriction site polymorphisms in cpDNA, all of which united geographical areas containing populations of both species. We detected no informative species‐specific markers. Studies of other species (e.g. oaks) have detected similar species‐independent geographical structure of cpDNA. However, in these cases secondary interegradation could be inferred from species‐specific nuclear alleles. The pattern in Ipomopsis is consistent with both primary intergradation (independent speciation in each area of sympatry) or secondary intergradation involving complete cytoplasmic replacement. Thus, additional data are needed to explain the origin of hybrid zones in Ipomopsis.

Distinguishing between primary and secondary intergradation among morphologically differentiated populations of Anolis marmoratus

Distinguishing between primary and secondary intergradation among differentiated populations, and the relative importance of drift and selection, are persistent problems in evolutionary biology. An historical perspective on population interactions can provide insight into the nature of contacts, and thus help resolve these questions. Continuously distributed populations of Anolis marmoratus from the island of Basse Terre in the Guadeloupean archipelago of the Lesser Antilles show a striking degree of geographic variation in morphology. Initial surveys of mtDNA variation from throughout the Guadeloupean Archipelago revealed one case where levels of sequence difference and phylogenetic relationships of alleles from morphologically differentiated populations from the east coast of Basse Terre were consistent with primary intergradation. In this paper, I examine the genetic population structure of a series of populations spanning this north-south cline in morphological variation to test the hypothesis of primary intergradation. Sequences of the mitochondrial cytochrome-b gene from 50 individuals representing five populations spanning the cline were obtained and fourteen unique haplotypes (differing by 2% or less) were detected. Patterns of nucleotide substitution among haplotypes do not deviate from neutral expectation indicating no effect of selection at the level of mtDNA sequences. Estimates of population structure and gene flow were made using both summary statistics for nucleotide diversity (Nst) and cladistic methods. The results are sensitive to the choice of gene flow model, and this is discussed in detail. Mitochondrial variation in the northern populations may not be at equilibrium, and the phylogeny of alleles is consistent with a recent increase in effective population size. Estimates of nucleotide diversity, gene flow, and the phylogenetic relationships of haplotypes indicate that the southern-most population (representing the extreme of morphological variation along this cline) has been relatively isolated from populations to the north and has experienced a reduced effective population size. The apparent clinal variation between the southern population and the others may therefore reflect secondary contact and introgression rather than primary intergradation.

Distinguishing between primary and secondary intergradation among morphologically differentiated populations of Anolis marmoratus

Distinguishing between primary and secondary intergradation among morphologically differentiated populations of Anolis marmoratus

Relictual Intergrades between the Northern Prairie Lizard (Sceloporus undulatus garmani) and the Red-Lipped Plateau Lizard (S. u. erythrocheilus) in Colorado

An isolated, relic population of intergrades between the northern prairie lizard (Sceloporus undulatus garmani) and the red-lipped plateau lizard (S. u. erythrocheilus) occurs in a very limited habitat in northeastern Elbert Co., Colorado, completely sur- rounded by habitats unsuitable for either subspecies. It is suggested that the two subspecies were in contact during two hypsithermal periods, separated by a hypo- thermal period, several thousand years ago, when first primary and later secondary intergradation occurred. The ensuing hypothermal period apparently eliminated all geographical and populational intermediates except those in this very restricted and particularly favorable habitat where a small population of the formerly widespread intergrades has managed to survive. Two subspecies of the eastern fence lizard (Sceloporus undulatus) occur in eastern Col-

Genetic Variation in Fundulusheteroclitus: Geographic Distribution

Studies of 16 polymorphic loci in the fish Fundulus heteroclitus have uncovered significant directional changes in gene frequencies with latitude (i.e., clines). These spatial patterns could have arisen by primary and/or secondary intergradation. While we cannot presently distinguish between these two models, mitochondrial DNA analyses indicate that if previous isolation occurred as required for secondary intergradation, it must have been relatively recent and of short duration. Herein we discuss the roles of genetic drift, random migration, nonrandom migration, selection and others as potential driving forces for both modes of cline formation. In addition, we address the potential role of the last glacial period in (1) creating isolating barriers, (2) the opening of unoccupied habitats for range extension, and (3) as a mechanism for thermal selection. While some evidence exists that at least one of the driving forces is selection, the extent to which it and other deterministic forces participate as opposed to various stochastic processes must await further analysis

Variation in the Eucalyptus gunnii-archeri Complex. II. The Origin of Variation

Previous studies of the Eucalyptus gunnii-archeri complex indicate marked differentiation of the adult phenotype. In this study, genetically based variation in the seedling phenotype is demonstrated. The five main phenetic groups in the complex are shown to be genetically defined and account for most of the genetic variation between populations. Further, the two major phenetic clines in the adult phenotype are paralleled by genetically based clines in the seedling phenotype, with greater genetic differentiation occurring along the cline between subspp. archeri and gunnii than along the cline between altitudinal extremes within subsp. gunnii. Detailed analyses of the structure of populations along the former continuum indicate no evidence for recent secondary intergradation since intermediate phenotypes are widespread and genetically stable and the various character clines appear to be independent. However, historical and biogeographical evidence is presented which suggests that a suture zone occurred between southern and northern populations during the last Pleistocene glacial. The area occupied by intermediate populations would have been amongst the last to be colonized following deglaciation. It is argued that extreme morphs differentiated in allopatry and that the continuum between the subspecies is a result of selective stabilization of a zone of secondary intergradation as opposed to primary intergradation. In contrast, the altitudinal continuum within subsp. gunnii appears to be mainly a result of primary differentiation within a population migrating up slope from a southern glacial refuge. Progeny trials indicate that the high variability and differentiation of several low-altitude, relic populations may be due to hybridization with surrounding species, whereas hybridization has little effect at the boundary of large stands. It is argued that hybridization may be important in the process of range contraction and extinction, and may be a significant evolutionary stimulus in small peripheral isolates.

Types of hybrid zones

Abstract Three types of hybrid zones may be recognized from their origin and evolutionary significance: Mayr's zones of primary intergradation between geographical races; secondary overlap zones following a more or less prolonged isolation; and narrow overlappings of parapatric populations differing in their karyotype. This third type may be the expression of stasipatric or of invasive patterns of chromosomal speciation. For some mammals and grasshoppers with parapatric hybrid zones it has been possible to identify the number and kind of chromosomal rearrangements involved and to estimate the time of fission between incipient species and the geographical pattern of speciation. The narrowness of the parapatric hybrid zones is due to the low vagility of the organisms concerned and/or to the lowered viability or fertility of the hybrids. The future of the hybrid zones seems to be quite undetermined and possibly very different in the different instances.

Intra-Island Variation in the 'Elepaio on the Island of Hawai'i

The 'Elepaio (Chasiempis sandwichensis) exhibits great vari- ation in plumage color on the Island of Hawai'i. Analysis of specimens from localities throughout the island reveals that the variation is geographically based, and that three subspecies can be distinguished: C. s. bryani, a pale form found at high elevation on the southwestern slopes of Mauna Kea; C. s. ridgwayi, a dark form found in wet windward forests; and C. s. sandwich- ensis, an intermediate form found in forests of the Kona region. Several zones of primary intergradation and one of possibly secondary intergradation occur, but appear to be narrow. The forms C. s. sclateri of Kaua'i and C. s. gayi of O'ahu exhibit no similar intra-island variation. Variation among the Hawai'i subspecies probably evolved in response to local variation in rainfall, and follows the predictions of Gloger's Rule, but the selective forces involved are obscure. The 'Elepaio (Chasiempis sandwichensis) is a monarchine flycatcher that comprises a genus endemic to the Hawaiian Islands. 'Elepaios occur on Kaua'i, O'ahu, and Ha- wai'i, but are enigmatically absent from oth- er seemingly suitable islands. Great plum-