Hybrid speciation is for the birds (and plants, reptiles, fish, and insects)

The Italian sparrow

The Italian sparrow, Passer italiae, a hybrid species whose parentals are the house sparrow, Passer domesticus, and the Spanish sparrow, Passer hispaniolensis. Photo courtesy of Alessandro Landi

R. A. Fisher once called hybridization ‘‘the grossest blunder in sexual preference which we can conceive of an animal making.” While there may be negative fitness consequences for an individual who mates across species boundaries, the evolutionary significance of hybridization in speciation, introgression, and adaptive radiation is a fascinating question gaining research attention, particularly given the relative ease with which we can now collect genomic data.

Hybridization can lead to a reduction in biodiversity through “despeciation.” If we consider species to be distinct, relatively stable, genotypic clusters, it is easy to imagine that ecological or geographical change may facilitate gene flow sufficient to homogenize both species into one cluster if reproductive barriers are weak. Examples of species fusion include Darwin’s finches and cichlid fish.

In some cases, hybridization can lead to establishment of a new, third species, hence increasing biodiversity. Keeping with our definition of species as genotypic clusters, the hybrid species would be a third cluster of genotypes that remains distinct even when in contact with the parental species.

 

Hybrid speciation can proceed instantaneously through the duplication of the hybrid’s genome (i.e. allopolyploidy, Figure 1a and 1b below adapted from Abbott and Rieseberg 2012). Hybrid speciation through allopolyploidy has been confirmed experimentally in many plant species and is now recognized as a prominent mechanism of speciation in flowering plants and ferns (Soltis et al. 2010).

Figure 1: (a) Allotetraploid formation through genome doubling of a sterile F1 hybrid between two diploid species. (b) Allotetraploid formation through fusion of unreduced gametes produced by two hybridizing diploid species. Adapted from Abbott and Rieseberg (2012)

Figure 1: (a) Allotetraploid formation through genome doubling of a sterile F1 hybrid between two diploid species. (b) Allotetraploid formation through fusion of unreduced gametes produced by two hybridizing diploid species. Figure and caption from Abbott and Rieseberg (2012)

Hybrid speciation can also proceed without a doubling in chromosome number (i.e. homoploid hybrid speciation). Homoploid hybrids are not immediately reproductively isolated from their parent species so although they are more likely to form than polyploid hybrid species, they are less frequent in nature because new hybrid genotypes are often overcome by gene flow from their parents before they become stabilized. Homoploid hybrid speciation presents an interesting paradox- gene flow must occur between the parental species for the hybrid to form but there must be some degree of isolation for the hybrid species to remain distinct from the parentals.

Because intrinsic reproductive barriers are initially weak, other isolating mechanisms, such as ecological or geographic divergence, are thought to be important to the establishment of homoploid hybrids. For example, “hybrids often exhibit expanded ecological tolerances, and all homoploid hybrid species that have been documented are ecologically divergent from their parental species. Likewise, spatial isolation provided by hybrid founder events may allow hybrid genomes to become stabilised before they are overcome by gene flow (Abbott and Rieseberg 2012).” Hybridization among sunflower species is an excellent case for genetically documented homoploid hybrid speciation (Reiseberg et al 2003).

The formation of a new sunflower species. Hybridization among sunflower species constitutes currently the genetically best documented case for homoploid hybrid speciation. The photograph shows the two parental species (on the left and right) that have hybridized to give rise to a new species (in the centre). Note that the new species grows in a habitat (i.e. the desert) that would not be accessible to either parental species. The initial hybridization event occurred 50 000 years ago and chromosomal inversions have contributed to the stabilization of the hybrid species within the first few hundred generations. Artificial crosses among the parental species result in hybrid lineages that can also occupy the desert environment, suggesting that the alleles that have contributed to the hybrid species are still part of the current gene pool of the parental species.

Figure 2: The formation of a new homoploid hybrid sunflower species. The photograph shows the two parental species (on the left and right) that have hybridized to form a new species (in the center). Note that the new species grows in a habitat (i.e. the desert) not accessible to either parental species. Photo and caption from Nolte and Tautz 2010

When hybrid species are spatially isolated from their parental species, intrinsic reproductive barriers can be difficult to study due to lack of geographical contact between taxa; we know little about whether pre-existing incompatibilities between parental species may contribute to reproductive isolation under homoploid hybrid speciation. In two papers published in 2014, Trier et al. (PLoS Genetics) and Hermansen et al. (Molecular Ecology) empirically test for intrinsic reproductive isolation among the homoploid hybrid Italian sparrow and its parental species, the Spanish and house sparrows, with which the Italian sparrow overlaps geographically.

The Italian sparrow is in contact with the house sparrow in a stable, narrow hybrid zone in the Alps and with the Spanish sparrow in a recently established sympatric zone in southeast Italy. In Sardinia, off the west coast of Italy, Spanish sparrows occur allopatrically [see Figure 3 in this post]. House and Spanish sparrows are themselves broadly, and often locally, sympatric across the entire Spanish sparrow range, remaining phenotypically distinct in all but a few locations. Hence reproductive barriers exist and are typically effective in maintaining isolation between the parent species, but can be broken down to form viable hybrid populations and species. -Trier et al. 2014

Figure 3. Phenotypic and genetic makeup of the hybrid Italian sparrow. Coloration of the map denotes phenotypic distribution as indicated by the bird drawings to the right of the map (blue: house sparrow, turquoise: Italian-house hybrids, yellow: typical Italian sparrow, orange: Italian sparrows with plumage intermediate between typical Italian and Spanish sparrows, red: Spanish sparrow). Bird drawings indicate species-specific male plumage characteristics of the three taxa [16]. Pie charts denote mean hybrid index at sampling localities where white and black color indicate house and Spanish sparrow genetic contribution, respectively. Locations with evidence of recent gene exchange between Spanish and Italian sparrows are indicated by arrows. Figure and caption courtesy of Trier et al 2014

Figure 3. Phenotypic and genetic makeup of the hybrid Italian sparrow. Coloration of the map denotes phenotypic distribution as indicated by the bird drawings to the right of the map (blue: house sparrow, turquoise: Italian-house hybrids, yellow: typical Italian sparrow, orange: Italian sparrows with plumage intermediate between typical Italian and Spanish sparrows, red: Spanish sparrow). Bird drawings indicate species-specific male plumage characteristics of the three taxa. Pie charts denote mean hybrid index at sampling localities where white and black color indicate house and Spanish sparrow genetic contribution, respectively. Locations with evidence of recent gene exchange between Spanish and Italian sparrows are indicated by arrows. Figure and caption from Trier et al 2014

Trier et al. generated a set of putatively parent species-specific SNP markers located in nuclear and mitochondrial genes and genotyped individuals from all three species (n = 612 birds in total). The authors used a cline analysis approach to identify candidate reproductive isolation (RI) genes that may drive homoploid hybrid speciation in the Italian sparrow. If markers with clines falling on current hybrid-parental boundaries are disproportionately Z/sex-linked (in birds females are heterogametic in a ZZ/ZW sex chromosome system), this suggests intrinsic RI while if markers with clines falling on current hybrid-parental boundaries are disproportionally autosomal then this suggests ecological divergence is a more likely mechanism of hybrid speciation in the Italian sparrow.

Results of the cline analysis showed “a disproportionately large number of sex-linked genes, as well as the mitochondria and nuclear genes with mitochondrial function, exhibit sharp clines at the boundaries between the hybrid and the parent species, suggesting a role for mito-nuclear and sex-linked incompatibilities in forming reproductive barriers (Trier et al. 2014).” Briefly, intrinsic genetic incompatibilities are a more likely mechanism of hybrid speciation in the Italian sparrow than ecological ones. The authors go on to hypothesize that the same loci involved in RI between the the Italian sparrow and its parental species will be a subset of those loci responsible for RI between the Spanish and house sparrows. Alternatively, it is possible that RI between hybrids and their parental species is the result of novel genetic incompatibles. If you are curious to know the answer, wait no longer because in a subsequent paper, Hermansen et al. tested these predictions empirically.

To what extent intrinsic barriers separating hybrids from their parents develop through sorting of pre-existing parental incompatibilities or through de-novo epistatic interactions in the hybrid genomes therefore remains an open question. This question can, however–as suggested by Rieseberg (1997)–be addressed by comparing the locations of genomic regions contributing to intrinsic reproductive barriers between the parent species with those isolating the hybrid species from their parents. If the genomic regions contributing to reproductive isolation in a hybrid taxon are a subset of those acting between its parents, then the sorting hypothesis would be supported. -Hermansen et al. 2014

Using data from Trier et al. 2014 and newly generated data for parental species collected from the Iberian Peninsula, Hermansen et al. compared SNP loci exhibiting restricted introgression at the range boundaries between the hybrid Italian sparrow and its parent species to loci exhibiting restricted introgression in an area where the parent species co-occur and hybridize.

The authors found that consistent with the prediction from the sorting hypothesis, the five Z-linked candidate RI loci identified by Trier et al. between the Italian sparrow and its parent species were among the 19 loci exhibiting restricted introgression in parental sympatry. Hermansen et al. also found 10 autosomal loci with restricted introgression between sympatric house and Spanish sparrows, which supports the sorting hypothesis that hybrid–parent RI genes should represent a subset of parent–parent RI genes. Interestingly, one autosomal marker, RPS4, identified by Trier et al. as a candidate RI locus between the hybrid Italian sparrow and the Spanish sparrow did not exhibit a significantly steep cline between sympatric house and Spanish sparrows, suggesting this marker may be a novel RI locus that developed de novo between the Italian and Spanish sparrows.

Fisher, R. A. The Genetical Theory of Natural Selection (Clarendon Press, Oxford, 1930).

Grant, B. R., & Grant, P. R. (1996). High survival of Darwin’s finch hybrids: effects of beak morphology and diets. Ecology, 77, 500-509. DOI: 10.2307/2265625

Seehausen, O., van Alphen, J. J., & Witte, F. (1997). Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277(5333), 1808-1811. DOI: 10.1126/science.277.5333.1808

Abbott, Richard J; and Rieseberg, Loren H (2012) Hybrid Speciation. In: eLS. John Wiley & Sons, Ltd: Chichester. DOI: 10.1002/9780470015902.a0001753.pub2

Soltis, D. E., Buggs, R. J., Doyle, J. J., & Soltis, P. S. (2010). What we still don’t know about polyploidy. Taxon, 59 (5), 1387-1403. http://www.jstor.org/stable/20774036

Rieseberg, L. H., Raymond, O., Rosenthal, D. M., Lai, Z., Livingstone, K., Nakazato, T., … & Lexer, C. (2003). Major ecological transitions in wild sunflowers facilitated by hybridization. Science, 301(5637), 1211-1216.DOI: 10.1126/science.1086949 

Nolte, A. W., & Tautz, D. (2010). Understanding the onset of hybrid speciation.Trends in Genetics, 26(2), 54-58. DOI: 10.1016/j.tig.2009.12.001

Trier, C. N., Hermansen, J. S., Sætre, G. P., & Bailey, R. I. (2014). Evidence for mito-nuclear and sex-linked reproductive barriers between the hybrid Italian sparrow and its parent species. PLoS Genetics, 10(1), e1004075. DOI: 10.1371/journal.pgen.1004075.g001

Hermansen, J. S., Haas, F., Trier, C. N., Bailey, R. I., Nederbragt, A. J., Marzal, A., & Sætre, G. P. (2014). Hybrid speciation through sorting of parental incompatibilities in Italian sparrows. Molecular Ecology, 23(23), 5831-5842. DOI: 10.1111/mec.12910

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About Melissa DeBiasse

I am a postdoctoral researcher at the University of Florida Whitney Laboratory for Marine Bioscience. As an evolutionary ecologist I am interested in the processes that generate biodiversity in marine ecosystems. My research uses experimental methods and genomic and phenotypic data to test how marine invertebrate species respond to biotic and abiotic stressors over ecological and evolutionary timescales.
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