Haldane's rule in an avian system: using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal, and sex-linked loci across the Passerina bunting hybrid zone

Using cline fitting and divergence population genetics, we tested a prediction of Haldane's rule: autosomal alleles should introgress more than z-linked alleles or mitochondrial haplotypes across the Passerina amoena/Passerina cyanea (Aves: Cardinalidae) hybrid zone. We screened 222 individuals collected along a transect in the Great Plains of North America that spans the contact zone for mitochondrial (two genes), autosomal (four loci) and z-linked (two loci) markers. Maximum-likelihood cline widths estimated from the mitochondrial (223 km) and z-linked (309 km) datasets were significantly narrower on average than the autosomal cline widths (466 km). We also found that mean coalescent-based estimates of introgression were larger for the autosomal loci (0.63 genes/generation, scaled to the mutation rate mu) than for both the mitochondrial (0.27) and z-linked loci (0.59). These patterns are consistent with Haldane's rule, but the among-locus variation also suggests many independently segregating loci are required to investigate introgression patterns across the genome. These results provide the first comprehensive comparison of mitochondrial, sex-linked, and autosomal loci across an avian hybrid zone and add to the body of evidence suggesting that sex chromosomes play an important role in the formation and maintenance of reproductive isolation between closely related species.     

Speciation in Passerina buntings: introgression patterns of sex-linked loci identify a candidate gene region for reproductive isolation

Sex-chromosomes are thought to play an important role in speciation, but few studies of non-model organisms have investigated the relative influence of multiple sex-linked markers on reproductive isolation. We collected 222 individuals along a geographical transect spanning the hybrid zone between Passerina amoena and P. cyanea (Aves: Cardinalidae). Using maximum-likelihood cline fitting methods, we estimated locus-specific introgression rates for 10 z-linked markers. Although the cline width estimates ranged from 2.8 to 584 km, eight of 10 loci had cline widths between 224 and 271 km. We also used coalescent-based estimates of locus-specific divergence times between P. amoena and P. cyanea to test a recently proposed hypothesis of an inverse relationship between divergence time and cline width but did not find a significant association. The narrow width (2.8 km) of the cline estimated from the VLDLR9 locus indicates strong selection retarding introgression of alleles at this locus across the hybrid zone. Interestingly, a mutation in the very low density lipoprotein receptor ( VLDLR ) gene, in which VLDLR9 is an intron, is known to reduce the egg-laying ability of some chickens, suggesting a possible link between this gene region and reproductive isolation between P. amoena and P. cyanea . These results underscore the importance of sampling multiple loci to investigate introgression patterns across a chromosome or genome and support previous findings of the importance of sex-linked genes in speciation.     

Development of RAPD markers in two introduced fire ants, Solenopsis invicta and S. richteri, and their application to the study of a hybrid zone

We developed RAPD DNA markers useful in distinguishing the fire ants Solenopsis invicta and S. richteri. An initial survey of 200 primers revealed seven informative markers; family studies allowed us to determine expression patterns and to confirm Mendelian inheritance of these markers. The seven RAPD markers, one of which is inherited as a codominant marker, were employed along with three allozyme markers to describe the structure of a hybrid zone that has formed between the two species in the USA, where they have been introduced. The data suggest minor introgression of alleles from one parental species ( S. richteri ) into the other ( S. invicta ), which most likely reflects the documented recent movement of this hybrid zone. This pattern is interpreted as interspecific introgression rather than shared intraspecific polymorphism on the basis of comparisons with samples from native, non-hybridizing populations in South America that lack such polymorphism. The data further reveal that the structure of the hybrid zone in the USA varies geographically. One parental species ( S. invicta ) and the hybrids exhibit a mosaic distribution in the east; a gradual transition between the parental species occurs in the centre, with a large intervening area of hybrid genotypes only; and there is apparent contact between parental populations with a small or no intervening zone of hybridization in the west. These differing patterns in the structure of the hybrid zone presumably reflect the unique histories of colonization in different parts of the range of introduced fire ants.     

SPATIO‐TEMPORAL CHANGES IN THE STRUCTURE OF AN AUSTRALIAN FROG HYBRID ZONE: A 40‐YEAR PERSPECTIVE

Spatio‐temporal studies of hybrid zones provide an opportunity to test evolutionary hypotheses of hybrid zone maintenance and movement. We conducted a landscape genetics study on a classic hybrid zone of the south‐eastern Australian frogs, Litoria ewingii and Litoria paraewingi. This hybrid zone has been comprehensively studied since the 1960s, providing the unique opportunity to directly assess changes in hybrid zone structure across time. We compared both mtDNA and male advertisement call data from two time periods (present and 1960s). Clinal analysis of the coincidence (same center) and concordance (same width) of these traits indicated that the center of the hybrid zone has shifted 1 km south over the last 40 years, although the width of the zone and the rate of introgression remained unchanged. The low frequency of hybrids, the strong concordance of clines within a time period, and the small but significant movement across the study period despite significant anthropogenic changes through the region, suggest the hybrid zone is a tension zone located within a low‐density trough. Hybrid zone movement has not been considered common in the past but our findings highlight that it should be considered a crucial component to our understanding of evolution.     

Evidence for concerted movement of nuclear and mitochondrial clines in a lizard hybrid zone

Moving hybrid zones provide compelling examples of evolution in action, yet long‐term studies that test the assumptions of hybrid zone stability are rare. Using replicated transect samples collected over a 10‐year interval from 2002 to 2012, we find evidence for concerted movement of genetic clines in a plateau fence lizard hybrid zone (Sceloporus tristichus) in Arizona. Cline‐fitting analyses of SNP and mtDNA data both provide evidence that the hybrid zone shifted northward by approximately 2 km during the 10‐year interval. For each sampling period, the mtDNA cline centre is displaced from the SNP cline centre and maintaining an introgression distance of approximately 3 km. The northward expansion of juniper trees into the Little Colorado River Basin in the early 1900s provides a plausible mechanism for hybrid zone formation and movement, and a broadscale quantification of recent land cover change provides support for increased woody species encroachment at the southern end of the hybrid zone. However, population processes can also contribute to hybrid zone movement, and the current stability of the ecotone habitats in the centre of the hybrid zone suggests that movement could decelerate in the future.     

HISTORICAL DIVERGENCE AND GENE FLOW: COALESCENT ANALYSES OF MITOCHONDRIAL,AUTOSOMAL AND SEX‐LINKED LOCI IN PASSERINA BUNTINGS

Quantifying the role of gene flow during the divergence of closely related species is crucial to understanding the process of speciation. We collected DNA sequence data from 20 loci (one mitochondrial, 13 autosomal, and six sex‐linked) for population samples of Lazuli Buntings (Passerina amoena) and Indigo Buntings (Passerina cyanea) (Aves: Cardinalidae) to test explicitly between a strict allopatric speciation model and a model in which divergence occurred despite postdivergence gene flow. Likelihood ratio tests of coalescent‐based population genetic parameter estimates indicated a strong signal of postdivergence gene flow and a strict allopatric speciation model was rejected. Analyses of partitioned datasets (mitochondrial, autosomal, and sex‐linked) suggest the overall gene flow patterns are driven primarily by autosomal gene flow, as there is no evidence of mitochondrial gene flow and we were unable to reject an allopatric speciation model for the sex‐linked data. This pattern is consistent with either a parapatric divergence model or repeated periods of allopatry with gene flow occurring via secondary contact. These results are consistent with the low fitness of female avian hybrids under Haldane's rule and demonstrate that sex‐linked loci likely are important in the initial generation of reproductive isolation, not just its maintenance.     

The phylogenetic affinities of the Socotra Bunting Emberiza socotrana

The monophyly of the African ‘brown bunting’ complex was corroborated by a recent molecular study. However, the little-known Socotran endemic Emberiza socotrana, which is morphologically similar to the other taxa in this complex, was not included. Here we present a hypothesis of the phylogenetic relationships of the Socotra Bunting based on one mitochondrial gene and one nuclear intron. We found the Socotra Bunting to be deeply nested within the African ‘brown bunting’ complex and, although morphologically most similar to E. capensis, it proved to be more closely related to the E. striolata/sahari and E. tahapisi/goslingi species groups. The phylogenetic uniqueness of the Socotra Bunting underpins once more the evolutionary importance of the Endemic Bird Area of Socotra, which is often considered the ‘Galápagos of the Indian Ocean’.     

A hybrid zone revisited: molecular and morphological analysis of the maintenance, movement, and evolution of a Great Plains avian (Cardinalidae: Pheucticus) hybrid zone

Black-headed grosbeaks ( Pheucticus melanocephalus ) and rose-breasted grosbeaks ( Pheucticus ludovicianus ) are passerine bird species known to hybridize in the Great Plains of North America. Both extrinsic (environmental) and intrinsic factors (pre- and postzygotic reproductive isolation) have been credited for the generation and maintenance of the grosbeak hybrid zone, but little is known about the genetic characteristics of this hybrid zone. To investigate the stability and extent of the grosbeak hybrid zone, we constructed clines from both molecular sequence data (mtDNA, three autosomal intron loci, and one Z-linked locus) and morphological data (morphometric analyses and hybrid index scores) to determined zone centre and width. Hybrid zone centre and width were also determined for samples collected across the zone 40 years ago from morphological data. The present and past clines were compared and provided support for stability in hybrid zone location and width, and the evolutionary implications of this are discussed. Three models of hybrid zone maintenance were investigated to consider the influence of intrinsic and extrinsic factors on this zone. Our results suggest low hybrid frequencies, a stable zone location and narrow width, and reduced hybrid fitness over the past 40 years best categorize the grosbeak hybrid zone as a tension zone.     

Empirical study of hybrid zone movement

Hybrid zones are 'natural laboratories' for studying the origin, maintenance and demise of species. Theory predicts that hybrid zones can move in space and time, with significant consequences for both evolutionary and conservation biology, though such movement is often perceived as rare. Here, a review of empirical studies of moving hybrid zones in animals and plants shows 23 examples with observational evidence for movement, and a further 16 where patterns of introgression in molecular markers could be interpreted as signatures of movement. The strengths and weaknesses of methods used for detecting hybrid zone movement are discussed, including long-term replicated sampling, historical surveys, museum/herbarium collections, patterns of relictual populations and introgression of genetic markers into an advancing taxon. Factors governing hybrid zone movement are assessed in the light of the empirical studies, including environmental selection, competition, asymmetric hybridization, dominance drive, hybrid fitness, human activity and climate change. Hybrid zone movement means that untested assumptions of stability in evolutionary studies on hybrid zone can lead to mistaken conclusions. Movement also means that conservation effort aimed at protecting against introgression could unwittingly favour an invading taxon. Moving hybrid zones are of wide interest as examples of evolution in action and possible indicators of environmental change. More long-term experimental studies are needed that incorporate reciprocal transplants, hybridization experiments and surveys of molecular markers and population densities on a range of scales.     

Effect of cereal harvesting method on a recent population decline of Corn Buntings Emberiza calandra on the Western Isles of Scotland

Capsule Population decline since 1995 is associated with the harvesting of cereals as arable silage.

Aim To survey Corn Bunting populations on the Western Isles and test whether population changes since 1995 are associated with change in cereal harvesting methods.

Methods Twelve areas of machair on the Uists and Benbecula were re-surveyed in 2002, after previous surveys in 1983 and 1995. These and other areas of suitable habitat on these islands, plus Berneray, Baleshare, Vallay, Barra and Vatersay, were surveyed in 2003–05 to provide a breeding population estimate for the Western Isles. Cereal strips in the 12 core survey areas were mapped in 2002 and the timing and method of harvesting of each was recorded. Cattle-feeding stands in 24 crofting townships were visited in March 2003 to record the type of fodder available, measure grain abundance and ripeness in fodder samples, and record foraging Corn Buntings. Experimental trials tested whether Corn Buntings selected fodder with riper grain.

Results The Western Isles Corn Bunting population was estimated at 117 occupied territories in 2005, a decline of 17% since 2002/03, and of at least 62% since 1995. Population decline was greater in areas with higher proportions of the cereal area harvested as arable silage. Arable silage contained fewer and less-ripe grains than traditionally harvested cereal, and was less likely to attract feeding Corn Buntings. Corn Buntings preferred to feed on silage containing riper grain.

Conclusions The remaining Corn Bunting population of the Western Isles is declining rapidly, probably because of reduction in winter grain supply caused by change from traditional reaper-binder harvesting and stacking of fully ripe cereals to harvesting the crop as unripe or partially ripe arable silage. Management change to restore a supply of ripe grain over winter is likely to be essential if this population decline is to be halted and reversed.     

新疆黄鹀冬季的生物学资料

调查资料表明,黄鹀(Emberiza citronella erythrogenys)在中国境内新疆北部越冬,并非是偶见冬候鸟或迷鸟。     

Historical hybrid zone movement: More pervasive than appreciated

Hybrid zones are established where two divergent populations meet and interbreed, but experience some reproductive isolation. If one population expands its range at the expense of the other, their hybrid zone moves. While hybrid zone movement is generally considered to be uncommon and insignificant, recent studies challenge this idea. The commonality of contemporary hybrid zone movement—with shifts in hybrid zones tracked over years to decennia—cannot be disputed, given the many examples available. Cases of historical hybrid zone movement—covering centuries or millennia of mobility—are accumulating, with movement having been inferred from five lines of evidence: (1) range shifts documented in the fossil/pollen record; (2) distribution dynamics derived from species distribution modelling; (3) enclaves of a displaced population persisting inside the range of an expanding one; (4) a peak of linkage disequilibrium at the leading edge of a moving hybrid zone; and (5) genome‐wide genetic traces of a displaced population, left behind in an expanding one. While most of these lines of evidence are not straightforward to interpret and/or broadly applicable, the latter—a genomic footprint of hybrid zone movement—promises to be particularly suitable to determine whether a hybrid zone has been on the move since its inception. I argue that historical hybrid zone movement is likely to be prevalent and deserves wider acknowledgement in historical biogeography.     

Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis

The study of hybrid zones is central to our understanding of the genetic basis of reproductive isolation and speciation, yet very little is known about the extent and significance of hybrid zones in marine fishes. We examined the population structure of cod in the transition area between the North Sea and the Baltic Sea employing nine microsatellite loci. Genetic differentiation between the North Sea sample and the rest increased along a transect to the Baltic proper, with a large increase in level of differentiation occurring in the Western Baltic area. Our objective was to determine whether this pattern was caused purely by varying degrees of mechanical mixing of North Sea and Baltic Sea cod or by interbreeding and formation of a hybrid swarm. Simulation studies revealed that traditional Hardy-Weinberg analysis did not have sufficient power for detection of a Wahlund effect. However, using a model-based clustering method for individual admixture analysis, we were able to demonstrate the existence of intermediate genotypes in all samples from the transition area. Accordingly, our data were explained best by a model of a hybrid swarm flanked by pure nonadmixed populations in the North Sea and the Baltic Sea proper. Significant correlation of gene identities across loci (gametic phase disequilibrium) was found only in a sample from the Western Baltic, suggesting this area as the centre of the apparent hybrid zone. A hybrid zone for cod in the ecotone between the high-saline North Sea and the low-saline Baltic Sea is discussed in relation to its possible origin and maintenance, and in relation to a classical study of haemoglobin variation in cod from the Baltic Sea/Danish Belt Sea, suggesting mixing of two divergent populations without interbreeding.     

Design and effectiveness of a novel trap for capturing nesting songbirds

ABSTRACT Capturing songbirds at their nests can be challenging and time consuming. Although traps designed for capturing songbirds at their nests have been described in the literature, few are effective for capturing species with open‐cup nests. We describe a cylindrical trap designed to capture songbirds at nests up to 2 m above ground in grasses, forbs, shrubs, and small saplings. The nest trap is constructed using a rigid hoop, two pieces of mist net, three stakes, and twist ties. We used this trap to capture female Dickcissels (Spiza americana) and female Indigo Buntings (Passerina cyanea) at their nests, with success rates of 85% (N= 196) and 60–73% (N= 16), respectively. Trapping success was comparable to that using other passerine nest trap designs. Nest abandonment after trapping attempts was rare and similar to that reported in previous studies. Our nest trap is lightweight, easy to make, versatile enough to use in a variety of grassland and shrub habitats, and easily carried and deployed in the field.     

Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone

Theory predicts that naturally occurring hybrid zones between genetically distinct taxa can move over space and time as a result of selection and/or demographic processes, with certain types of hybrid zones being more or less likely to move. Determining whether a hybrid zone is stationary or moving has important implications for understanding evolutionary processes affecting interactions in hybrid populations. However, direct observations of hybrid zone movement are difficult to make unless the zone is moving rapidly. Here, evidence for movement in the house mouse Mus musculus domesticus × Mus musculus musculus hybrid zone is provided using measures of LD and haplotype structure among neighbouring SNP markers from across the genome. Local populations of mice across two transects in Germany and the Czech Republic were sampled, and a total of 1301 mice were genotyped at 1401 markers from the nuclear genome. Empirical measures of LD provide evidence for extinction and (re)colonization in single populations and, together with simulations, suggest hybrid zone movement because of either geography-dependent asymmetrical dispersal or selection favouring one subspecies over the other.     

Species distribution models contribute to determine the effect of climate and interspecific interactions in moving hybrid zones

Climate is a major factor delimiting species’ distributions. However, biotic interactions may also be prominent in shaping geographical ranges, especially for parapatric species forming hybrid zones. Determining the relative effect of each factor and their interaction of the contact zone location has been difficult due to the lack of broad scale environmental data. Recent developments in species distribution modelling (SDM) now allow disentangling the relative contributions of climate and species’ interactions in hybrid zones and their responses to future climate change. We investigated the moving hybrid zone between the breeding ranges of two parapatric passerines in Europe. We conducted SDMs representing the climatic conditions during the breeding season. Our results show a large mismatch between the realized and potential distributions of the two species, suggesting that interspecific interactions, not climate, account for the present location of the contact zone. The SDM scenarios show that the southerly distributed species, Hippolais polyglotta, might lose large parts of its southern distribution under climate change, but a similar gain of novel habitat along the hybrid zone seems unlikely, because interactions with the other species (H. icterina) constrain its range expansion. Thus, whenever biotic interactions limit range expansion, species may become ‘trapped’ if range loss due to climate change is faster than the movement of the contact zone. An increasing number of moving hybrid zones are being reported, but the proximate causes of movement often remain unclear. In a global context of climate change, we call for more interest in their interactions with climate change.     

Genetic population structure of turbot (Scophthalmus maximus L.) supports the presence of multiple hybrid zones for marine fishes in the transition zone between the Baltic Sea and the North Sea

Genetic population structure of turbot (Scophthalmus maximus L.) in the Northeast Atlantic was investigated using eight highly variable microsatellite loci. In total 706 individuals from eight locations with temporal replicates were assayed, covering an area from the French Bay of Biscay to the Aaland archipelago in the Baltic Sea. In contrast to previous genetic studies of turbot, we found significant genetic differentiation among samples with a maximum pairwise FST of 0.032. Limited or no genetic differentiation was found among samples within the Atlantic/North Sea area and within the Baltic Sea, suggesting high gene flow among populations in these areas. In contrast, there was a sharp cline in genetic differentiation going from the low saline Baltic Sea to the high saline North Sea. The data were explained best by two divergent populations connected by a hybrid zone; however, a mechanical mixing model could not be ruled out. A significant part of the genetic variance could be ascribed to variation among years within locality. Nevertheless, the population structure was relatively stable over time, suggesting that the observed pattern of genetic differentiation is biologically significant. This study suggests that hybrid zones are a common phenomenon for marine fishes in the transition area between the North Sea and the Baltic Sea and highlights the importance of using interspecific comparisons for inferring population structure in high gene flow species such as most marine fishes.     

Quantifying the spatiotemporal dynamics in a chorus frog (Pseudacris) hybrid zone over 30 years

Although theory suggests that hybrid zones can move or change structure over time, studies supported by direct empirical evidence for these changes are relatively limited. We present a spatiotemporal genetic study of a hybrid zone between Pseudacris nigrita and P. fouquettei across the Pearl River between Louisiana and Mississippi. This hybrid zone was initially characterized in 1980 as a narrow and steep “tension zone,” in which hybrid populations were inferior to parentals and were maintained through a balance between selection and dispersal. We reanalyzed historical tissue samples and compared them to samples of recently collected individuals using microsatellites. Clinal analyses indicate that the cline has not shifted in roughly 30 years but has widened significantly. Anthropogenic and natural changes may have affected selective pressure or dispersal, and our results suggest that the zone may no longer best be described as a tension zone. To the best of our knowledge, this study provides the first evidence of significant widening of a hybrid cline but stasis of its center. Continued empirical study of dynamic hybrid zones will provide insight into the forces shaping their structure and the evolutionary potential they possess for the elimination or generation of species.     

Spring movements of Rüppell's Vulture Gyps rueppellii across the Strait of Gibraltar

Most of our understanding of territorial behaviour in birds comes from studies of temperate species. Territoriality and factors influencing territory size of tropical birds are still poorly studied. In this study, 11 territories of the Cinnamon-breasted Rock Bunting Emberiza tahapisi were measured in the Amurum Forest Reserve and adjoining farmlands. Factors influencing the habitat choice of this species were also studied. Territory sizes ranged from 0.1–0.3 ha with a mean territory size of 0.19 ± 0.1ha. Territory size decreased with increasing food abundance and increased with tree height and number of saplings. The birds did not show signs of territoriality in farmlands but flocked in small groups (mean group size 6.88 ± 0.89). Flock size also increased with increasing number of seeds. In the forested land, birds showed a preference for rocky outcrops, whereas in farmlands, they appeared to prefer open and newly cultivated farmlands with little or no ground cover. Understanding the influence of habitat variables on territory size and habitat selection in a locally abundant and widely distributed tropical species such as the Cinnamon-breasted Rock Bunting thus offers unique opportunities for understanding how changes in landscape caused by land-use regimes may affect populations.     

Variable visual habitats may influence the spread of colourful plumage across an avian hybrid zone

Several studies have shown that hybridization can be a creative process by acting as a conduit for the spread of adaptive traits between species, but few provide the mechanism that favours this spread. In the hybrid zone between the golden- (Manacus vitellinus) and white-collared (Manacus candei) manakins, sexual selection drives the introgression of golden/yellow plumage into the white species; however, the mechanism for the yellow male's mating advantage and the reasons why yellow plumage has not swept further into the white species remain mostly speculative. We quantified the colour properties of male plumage, the background and the ambient light at the hybrid zone, and allopatric golden and white populations. As measured by the perceived difference in colour between plumage and background, we found that yellow plumage appears more conspicuous than white plumage in the hybrid zone and allopatric golden-collar habitats, whereas white plumage appears more conspicuous than yellow plumage in the allopatric white-collared habitat. These results suggest a mechanism for the unidirectional spread of yellow plumage across the hybrid zone but slowed movement beyond it.