skip to main content


Title: Hybrid zone or hybrid lineage: a genomic reevaluation of Sibley’s classic species conundrum in Pipilo towhees
Abstract

Hybrid zones can be studied by modeling clines of trait variation (e.g., morphology, genetics) over a linear transect. Yet, hybrid zones can also be spatially complex, can shift over time, and can even lead to the formation of hybrid lineages with the right combination of dispersal and vicariance. We reassessed Sibley’s (1950) gradient between Collared Towhee (Pipilo ocai) and Spotted Towhee (Pipilo maculatus) in Central Mexico to test whether it conformed to a typical tension-zone cline model. By comparing historical and modern data, we found that cline centers for genetic and phenotypic traits have not shifted over the course of 70 years. This equilibrium suggests that secondary contact between these species, which originally diverged over 2 million years ago, likely dates to the Pleistocene. Given the amount of mtDNA divergence, parental ends of the cline have very low autosomal nuclear differentiation (FST = 0.12). Dramatic and coincident cline shifts in mtDNA and throat color suggest the possibility of sexual selection as a factor in differential introgression, while a contrasting cline shift in green back color hints at a role for natural selection. Supporting the idea of a continuum between clinal variation and hybrid lineage formation, the towhee gradient can be analyzed as one population under isolation-by-distance, as a two-population cline, and as three lineages experiencing divergence with gene flow. In the middle of the gradient, a hybrid lineage has become partly isolated, likely due to forested habitat shrinking and fragmenting as it moved upslope after the last glacial maximum and a stark environmental transition. This towhee system offers a window into the potential outcomes of hybridization across a dynamic landscape including the creation of novel genomic and phenotypic combinations and incipient hybrid lineages.

 
more » « less
Award ID(s):
1652979
NSF-PAR ID:
10401986
Author(s) / Creator(s):
; ; ; ; ; ;
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
Evolution
Volume:
77
Issue:
3
ISSN:
0014-3820
Format(s):
Medium: X Size: p. 852-869
Size(s):
["p. 852-869"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Numerous mechanisms can drive speciation, including isolation by adaptation, distance, and environment. These forces can promote genetic and phenotypic differentiation of local populations, the formation of phylogeographic lineages, and ultimately, completed speciation. However, conceptually similar mechanisms may also result in stabilizing rather than diversifying selection, leading to lineage integration and the long‐term persistence of population structure within genetically cohesive species. Processes that drive the formation and maintenance of geographic genetic diversity while facilitating high rates of migration and limiting phenotypic differentiation may thereby result in population genetic structure that is not accompanied by reproductive isolation. We suggest that this framework can be applied more broadly to address the classic dilemma of “structure” versus “species” when evaluating phylogeographic diversity, unifying population genetics, species delimitation, and the underlying study of speciation. We demonstrate one such instance in the Seepage Salamander (Desmognathus aeneus) from the southeastern United States. Recent studies estimated up to 6.3% mitochondrial divergence and four phylogenomic lineages with broad admixture across geographic hybrid zones, which could potentially represent distinct species supported by our species‐delimitation analyses. However, while limited dispersal promotes substantial isolation by distance, microhabitat specificity appears to yield stabilizing selection on a single, uniform, ecologically mediated phenotype. As a result, climatic cycles promote recurrent contact between lineages and repeated instances of high migration through time. Subsequent hybridization is apparently not counteracted by adaptive differentiation limiting introgression, leaving a single unified species with deeply divergent phylogeographic lineages that nonetheless do not appear to represent incipient species.

     
    more » « less
  2. Abstract

    Hybrid zones are natural experiments for the study of avian evolution. Hybrid zones can be dynamic, moving as species adjust to new climates and habitats, with unknown implications for species and speciation. There are relatively few studies that have comparable modern and historic sampling to assess change in hybrid zone location and width over time, and those studies have generally found mixed results, with many hybrid zones showing change over time, but others showing stability. The white‐throated magpie‐jay (Calocitta formosa) and black‐throated magpie‐jay (Calocitta colliei) occur along the western coast of Mexico and Central America. The two species differ markedly in throat color and tail length, and prior observation suggests a narrow hybrid zone in southern Jalisco where individuals have mixed throat color. This study aims to assess the existence and temporal stability of this putative hybrid zone by comparing throat color between georeferenced historical museum specimens and modern photos from iNaturalist with precise locality information. Our results confirm the existence of a narrow hybrid zone in Jalisco, with modern throat scores gradually increasing from the parental ends of the cline toward the cline center in a sigmoidal curve characteristic of hybrid zones. Our temporal comparison suggests that the hybrid zone has not shifted its position between historical (pre‐1973) and modern (post‐2005) time periods—a surprising result given the grand scale of habitat change to the western Mexican lowlands during this time. An anomalous pocket of white‐throated individuals in the northern range of the black‐throated magpie‐jay hints at the possibility of prehistorical long‐distance introduction. Future genomic data will help disentangle the evolutionary history of these lineages and better characterize how secondary contact is affecting both the DNA and the phenotype of these species.

     
    more » « less
  3. Abstract

    Phenotypic differentiation plays an important role in the formation and maintenance of reproductive barriers. In some cases, variation in a few key aspects of phenotype can promote and maintain divergence; hence, the identification of these traits and their associations with patterns of genomic divergence is crucial for understanding the patterns and processes of population differentiation. We studied hybridization between thealbaandpersonatasubspecies of the white wagtail (Motacilla alba), and quantified divergence and introgression of multiple morphological traits and 19,437SNPloci on a 3,000 km transect. Our goal was to identify traits that may contribute to reproductive barriers and to assess how variation in these traits corresponds to patterns of genome‐wide divergence. Variation in only one trait—head plumage patterning—was consistent with reproductive isolation. Transitions in head plumage were steep and occurred over otherwise morphologically and genetically homogeneous populations, whereas cline centres for other traits and genomic ancestry were displaced over 100 km from the head cline. Field observational data show that social pairs mated assortatively by head plumage, suggesting that these phenotypes are maintained by divergent mating preferences. In contrast, variation in all other traits and genetic markers could be explained by neutral diffusion, although weak ecological selection cannot be ruled out. Our results emphasize that assortative mating may maintain phenotypic differences independent of other processes shaping genome‐wide variation, consistent with other recent findings that raise questions about the relative importance of mate choice, ecological selection and selectively neutral processes for divergent evolution.

     
    more » « less
  4. Populations of the non-migratory estuarine fish Fundulus heteroclitus inhabiting the heavily polluted New Bedford Harbour (NBH) estuary have shown inherited tolerance to local pollutants introduced to their habitats in the past 100 years. Here we examine two questions: (i) Is there pollution-driven selection on the mitochondrial genome across a fine geographical scale? and (ii) What is the pattern of migration among sites spanning a strong pollution gradient? Whole mitochondrial genomes were analysed for 133 F. heteroclitus from seven nearby collection sites: four sites along the NBH pollution cline (approx. 5 km distance), which had pollution-adapted fish, as well as one site adjacent to the pollution cline and two relatively unpolluted sites about 30 km away, which had pollution-sensitive fish. Additionally, we used microsatellite analyses to quantify genetic variation over three F. heteroclitus generations in both pollution-adapted and sensitive individuals collected from two sites at two different time points (1999/2000 and 2007/2008). Our results show no evidence for a selective sweep of mtDNA in the polluted sites. Moreover, mtDNA analyses revealed that both pollution-adapted and sensitive populations harbour similar levels of genetic diversity. We observed a high level of non-synonymous mutations in the most polluted site. This is probably associated with a reduction in N e and concomitant weakening of purifying selection, a demographic expansion following a pollution-related bottleneck or increased mutation rates. Our demographic analyses suggest that isolation by distance influences the distribution of mtDNA genetic variation between the pollution cline and the clean populations at broad spatial scales. At finer scales, population structure is patchy, and neither spatial distance, pollution concentration or pollution tolerance is a good predictor of mtDNA variation. Lastly, microsatellite analyses revealed stable population structure over the last decade. 
    more » « less
  5. Abstract

    As hybrid zones exhibit selective patterns of gene flow between otherwise distinct lineages, they can be especially valuable for informing processes of microevolution and speciation. The bumble bee,Bombus melanopygus, displays two distinct color forms generated by Müllerian mimicry: a northern “Rocky Mountain'’ color form with ferruginous mid‐abdominal segments (B.m.melanopygus) and a southern “Pacific'’ form with black mid‐abdominal segments (B.m.edwardsii). These morphs meet in a mimetic transition zone in northern California and southern Oregon that is more narrow and transitions further west than comimetic bumble bee species. To understand the historical formation of this mimicry zone, we assessed color distribution data forB.melanopygusfrom the last 100 years. We then examined gene flow among the color forms in the transition zone by comparing sequences from mitochondrial COI barcode sequences, color‐controlling loci, and the rest of the nuclear genome. These data support two geographically distinct mitochondrial haplogroups aligned to the ancestrally ferruginous and black forms that meet within the color transition zone. This clustering is also supported by the nuclear genome, which, while showing strong admixture across individuals, distinguishes individuals most by their mitochondrial haplotype, followed by geography. These data suggest the two lineages most likely were historically isolated, acquired fixed color differences, and then came into secondary contact with ongoing gene flow. The transition zone, however, exhibits asymmetries: mitochondrial haplotypes transition further south than color pattern, and both transition over shorter distances in the south. This system thus demonstrates alternative patterns of gene flow that occur in contact zones, presenting another example of mito‐nuclear discordance. Discordant gene flow is inferred to most likely be driven by a combination of mimetic selection, dominance effects, and assortative mating.

     
    more » « less