TREE coverTREE coverCover of Trends in Ecology and Evolution - Black-capped ChickadeeOur group primarily studies birds, but hybridization is a widespread phenomenon that is broadly relevant to the evolutionary history of many species. We have led and have been involved in a number of reviews and syntheses that explore various topics related to hybridization, speciation, and anthropogenic change.

   

 

Select Figures from Reviews

With increasing frequency, genome-spanning datasets are revealing that hybridization has played a role in the evolution of a diverse and globally distributed array of taxa. Though it is often hard to infer that ancient hybridization has played an adaptive role in the evolution of extant taxa, it certainly appears to be a common phenomenon. There are many taxa, including humans, for which there were no obvious reasons to suspect that hybridization played a role in their evolutionary history. Clarifying the importance of hybridization in the evolutionary history of these groups is an important next step in their study. Examples of hybridization are shown in a–h. a, Hybridization between coyotes and gray wolves in north America51. b, Polar bear and brown bear hybridization during the last glacial maximum55. c, Human and Neanderthal hybridization following expansion of humans out of Africa24. d, Baker’s yeast hybridization before whole genome duplication34. e, Common bean hybridization with wild ancestors in South America77. f, Chimpanzee and bonobo hybridization53. g, Rampant ancient hybridization between extant and extinct elephantids29. h, Ancient hybridization between Congolese and Nile cichlid lineages appears to have led to the evolution of the Lake Victoria Super Flock of haplochromine cichlids30. Credit: Melissa Hoyer (a,b); Croisy/ Depositphotos.com (c, human skull); Creativemarc/Depositphotos. com (c, Neanderthal skull); iLexx/Depositphotos.com (d); vvoennyy/ Depositphotos.com (e); Pierre Fidenci (f); David Toews (g); Ole Seehausen (h); chrupka/Depositphotos.com (map)

a–c, Many of the most convincing examples of adaptive introgression come from contemporary introgression events (a) or from traits with very clear adaptive function. For single loci of large effect (c), this is easier than for multigene traits (b). a, Liu et al.71 build on the work of Song et al.70, which reported introgression of genes involved in warfarin resistance from M. spretus to M. m. domesticus. Using 22 whole genomes, Liu et al.71 found evidence of three hybridization events, one ancient and two more recent, between M. spretus and M. m. domesticus. Importantly, they recovered the same introgressed region on chromosome 7 that contains Vkorc1, which is important for warfarin resistance, and find functional enrichment of olfactory receptors in introgressed regions. b, Suarez-Gonzalez et al.67 used whole-chromosome sequencing to investigate introgression and signals of selection of candidate genes involved in local adaptation from Populus balsamifera into Populus trichocarpa. Functional trait and gene expression analyses in a common garden setting reveal correlations between these genomic regions with traits that are adaptive at the northern range limit of P. trichocarpa, where the growing season is shorter (which leads to, for example, higher photosynthetic rates and faster growth). c, Jones et al.76 use a combination of whole-genome and whole-exome sequencing to demonstrate that cis-regulatory variation controls seasonal expression of the Agouti gene, which underlies seasonal coat color change in snowshoe hares. Their analyses indicate that the allele for brown coat color introgressed from the black-tailed jackrabbit and swept to high frequency in snowshoe hare populations in habitats with mild winters, where a brown coat color matches the winter background. d, The Heliconius Genome Consortium73 used whole-genome resequencing to document introgression between species, particularly of two genomic regions that control mimicry patterns between three species of Heliconius that are co-mimics. Heliconius butterflies are unpalatable to vertebrate predators and are considered a classic example of Mullerian mimicry: their warning color patterns enable multiple species to share the cost of predator education. Wing patterns are also important in mate selection.

An important component of documenting this form of speciation is providing evidence that hybridization itself led to reproductive isolation between the hybrid species and its parental taxa16. Although there are a growing number of reports of hybrid speciation in the literature, few systems have convincingly demonstrated the criteria outlined in Schumer et al.16. The two systems included here are recent examples of reported homoploid hybrid speciation that use whole genomes to clarify patterns of divergence and selection in hybrid lineages. Differentiating between homoploid hybrid speciation and introgression from ancient hybridization will be an important avenue of future research. a, Geospiza conirostris and Geospiza fortis hybridized to produce the Big Bird lineage87. b, Leducq et al.88,89 used whole-genome sequencing to investigate hybrid speciation in the budding yeast S. paradoxus. Credit: K. Thalia Grant and Peter R. Grant (a); iLexx/ Depositphotos.com (b)

(A) Spruce hybrid zones (Picea glauca 3 Picea engelmannii and Picea glauca 3 Picea sitchensis) [90]. The map to the right shows species distributions [indicated by dark gray (Picea sitchensis), medium gray (Picea engelmannii) and light gray (Picea glauca)] and locations of the two hybrid zones. The triangle on the left summarizes estimated gene flow between the three species. Line width roughly corresponds to the percentage of shared alleles. Broken lines indicate potential gene flow between two parental species and admixed individuals from the other hybrid zone. Climatic variables that are associated with each hybrid zone are indicated on the outside of the triangle. (B) Swallowtail butterfly hybrid zone (Papilio glaucus and Papillo canadensis) [13]. The map indicates the hybrid zone (broken line) running east to west across Wisconsin. Lines represent the extent and direction (north or south) of species-specific trait introgression from 1998 to 2011. (C) Chickadee hybrid zone (Poecile atricapillus and Poecile carolinensis) [7]. Locus specific allele frequencies are plotted against distance along a linear transect (geographic clines) from historical (gray) and contemporary (black) sampling. Average shift north of 11.5 km in 10 years.

The top panels represent northward shifts of a southern species (gray) and a northern species (white) for (A) clinal and (B) mosaic hybrid zones. The gray shading represents the northern range edge of the historical (light gray, broken line) and contemporary (dark gray, unbroken line) distributions of the southern species. Arrows highlight the shift in the species distribution. Lines 1 and 2 represent north–south transects across the hybrid zone. The change in the allele frequency of the northern species along each transect for historical (broken line) and contemporary (solid line) samples are plotted for the clinal hybrid zone (C) and the mosaic hybrid zone (D). The clinal hybrid zone forms an extensive and narrow zone of contact that extends east and west. In the mosaic hybrid zone, parental forms occupy distinct habitat patches in a heterogeneous landscape and hybridization occurs across patch boundaries. The patterns of variation in allele frequency differ depending on the transect. As the range of the southern species shifts north, habitat patches alter; patches disappear, new patches form and the area of each patch changes.

Each panel depicts expected clines for a hybrid zone that is maintained by local adaptation, premating barriers that prevent the formation of hybrids, or selection against hybrids. The black lines depict a locus under selection; one that contributes to local adaptation or reproductive barriers. The gray represents the expected range of cline shapes for unlinked neutral markers. (A) Classic geographic clines. (B) Genomic clines modeled using multinomial regression [80,98]. (C) Genomic clines modeled using either Barton’s concordance method [99], Bayesian genomic clines [100] or the log-logistic method [74].

Theoretical outcomes of hybridization are illustrated along with the frequency of each outcome following human-mediated habitat disturbance based on a systematic literature search. Although the outcomes are depicted as a unidirectional flow chart, there is ample evidence suggesting that outcomes are not necessarily permanent and that populations can fluctuate between outcomes over longer evolutionary timescales. Large circles (blue, yellow, and green) represent populations of individuals with the same genotype. Blue and yellow circles are parental populations, while green circles and green areas of overlapping circles represent hybrid individuals of mixed ancestry. Blue stars represent alleles from the blue population. Small black arrows denote introgressed alleles. The thick broken line indicates an anthropogenic disturbance that promotes hybridization. Following disturbance, the most commonly detected outcome is hybrid swarm. We depict a hybrid swarm with patterned blue, yellow, and green circles. These hypothetical populations contain the same alleles as the parental population but they have been combined into genomic and phenotypically different populations.

Synthesized from the literature, these are the main mechanisms by which human-mediated habitat disturbances cause hybridization. (A–C) Detail mechanisms that erode prezygotic reproductive barriers and lead to interbreeding between sister species (in gray). (D) A postzygotic mechanism that causes increased occurrence of hybrids due to increased hybrid fitness in human-modified habitats (in white). The species highlighted in (A–D) correspond with each of four case studies detailed in the main text. The predisturbance row depicts unaltered conditions where sister species are isolated by reproductive barriers. Text above the broken line, followed by a horizontal black arrow, specifies the habitat disturbance that has been documented causing interbreeding between normally reproductively isolated species. An explanation of the pre- and postdisturbance panels appears at bottom of the figure. (A) Males of two tree frog species, the barking tree frog (Hyla gratiosa) and the green tree frog (Hyla cinerea,) call from differing locations in shared pools. Following removal of vegetation, males call from same location, resulting in higher frequencies of heterospecific matings. (B) Two species of Banksia (Banksia hookeriana and Banksia prionotes) have different flowering times. Banksia prionotes blooms first (white bar) and, in undisturbed conditions, is temporally separately from B. hookeriana (black bar). After soil disturbance, the flowering time of B. prionotes is extended to overlap with the now-earlier flowering B. hookeriana. (C) In a heterogeneous light environment, female cichlids (Pundamilia nyererei) exhibit strong mate choice based on male color. In eutrophic lakes, where colors cannot be discriminated, females mate indiscriminately with males. Thin black arrows show the direction of mating. (D) In undisturbed habitats, parental ant species (Formica sp.) have higher fitness than hybrids. Following forest fragmentation, hybrid fitness increases, leading to an increase in the number of hybrids in the population.

(A–C) Recommended workflow for experimental assessment of mechanisms of human-mediated hybridization. Gray ruler denotes methods that use morphology. The double helix denotes methods that use genomic data. Birds (white, black, and gray) represent two hypothetical closely related avian species (white and black birds) that interbreed and produce hybrids (gray birds). (A) Initial step of observing hybridization. Top: two discrete species (white and black birds) are shown in unaltered habitat (solid-bordered box). Using morphology, hybrid individuals (gray birds) are detected in disturbed habitat (broken-lined box). Bottom: high-resolution genome sequencing reveals a hypothetical allele frequency difference between populations and within hybrids at a specific genomic location. (B) Suggested methods of quantifying hybridization. Top: hybrids can exhibit various levels of genomic admixture. Hypothetical chromosomes are depicted exhibiting different levels of genomic admixture, which depends on hybrid generation, recombination rate, and linkage disequilibrium. Bottom: hypothetical plots showing admixture (e.g., from STRUCTURE) from undisturbed (solid-bordered box, top) and disturbed (broken-lined box, bottom) habitats. Each bar represents one individual. The coloring of the bars denotes the probability of assignment to each species (white and black, respectively). The small black bracket denotes individuals with a mixed probability of assignment to either population (i.e., hybrid individuals). (C) The experimental set-up. Boxes on the left represent control (solid-bordered box) and manipulated (broken-lined boxes) plots. Here, resources have been altered in treatment plots: food availability increased (top), food availability decreased (middle), and food and nesting sites increased (bottom). Intermediate individuals (gray bird) will be quantified for all plots using both morphology and high-resolution genomic data. Hypothetical plots showing genomic admixture illustrate variation in hybrid frequency for different control and experimental plots. Small black brackets denote potential hybrids.

Publications

2019

Taylor SA, Larson EL. 2019. Insights from genomes into the evolutionary importance and prevalence of hybridization in nature. Nature Ecology and Evolution 3, 170-177. https://doi.org/10.1038/s41559-018-0777-y

2018

Theodosopoulos AN, Hund AK, Taylor SA. 2018. Parasites and host species barriers in animal hybrid zones. Trends in Ecology and Evolution 34: 19-30.

2017

+Toews DPL, +Hofmeister NR, Taylor SA. 2017. The evolution and genetics of carotenoid processing in animals. Trends in Genetics 33: 171-182.

2016

Taylor SA, Campagna L. 2016. Perspectives: Avian supergenes. Science 351: 446-447. PDF=

2015

+Toews DPL, +Campagna L, +Taylor SA, Balakrishnan CN, Baldassarre DT, Deane-Coe PE, Harvey MG, Hooper DM, Irwin DE, Judy CD, Mason NA, McCormack JE, McCracken KG, Oliveros CH, Safran RJ, Scordato E, Stryjewski KF, Tigano A, Uy AJ, Winger, B. 2015. Genomic approaches to understanding population divergence and speciation in birds. The Auk: Ornithological Advances 133: 13-30 http://dx.doi.org/10.1642/AUK-15-51.1 +Authors contributed equally.  PDF

Taylor SA, Larson EL, Harrison RG. 2015. Hybrid Zones: Windows on Climate Change. Trends in Ecology and Evolution 30: 398-406.
DOI: j.tree.2015.04.010  PDF