A summary of a recent debate in the journal Ecology and Evolution.
The future of the Golden-winged Warbler (Vermivora chrysoptera) is threatened by habitat loss. In addition, it runs the risk of being outcompeted and “out-hybridized” by the invading Blue-winged Warbler (V. cyanoptera). The interactions between these two closely related species have a long history of scientific research (summarized on the Parulidae page). However, it is still unclear how strong the level of reproductive isolation between these warblers is. Recent work by David Toews and his colleagues pointed to six genomic regions that are highly divergent between Golden-winged and Blue-winged Warblers, of which four are likely involved in feather development or pigmentation. These findings suggest that differences in plumage patterns could act as a strong reproductive barrier. The strength of this potential barrier can be tested by quantifying the frequency of mixed pairings between different plumage types, and following the reproductive success of hybrids (if there are any).
A recent study in the journal Ecology and Evolution performed these measurements and reported strong reproductive isolation between Golden-winged and Blue-winged Warblers. However, another team of researchers questioned these results and indicated potential pitfalls in the analyses, to which the original authors responded. In this blog post, I will try to summarize the main arguments in this interesting debate.
Strong Reproductive Isolation?
Let’s start with the first study. To determine the degree of reproductive isolation between Golden-winged Warbler and Blue-winged Warbler, John Confer and his colleagues aggregated data on social pairing from nine studies. Apart from the two pure phenotypes, the researchers also considered two hybrid phenotypes: the “Brewster’s Warbler” and the “Lawrence’s Warbler”. These phenotypes were initially described as distinct species before they were recognized as hybrids. According to the model of Kenneth Parkes (1951), “Brewster’s Warblers” are first-generation hybrids between genetically pure Golden-winged and Blue-winged Warblers, while the “Lawrence’s Warbler” can be produced by crossing two first-generation hybrids.
The analyses revealed a low level of hybridization. Only 14 out of 1680 (0.9%) Golden-winged Warblers and 14 out of 583 (2.4%) Blue-winged Warblers paired up with another phenotype. These patterns indicate high levels of behavioral isolation between the different plumage phenotypes. Next, the researchers turned to the breeding success of the hybrid phenotypes. The pairing success of “Brewster’s Warblers” (54%) was significantly smaller compared to the pure Golden-winged (83%) and Blue-winged Warblers (77%). These percentages suggest some degree of sexual selection against hybrids. Putting it all together, the researchers calculated a reproductive isolation score of 0.96. Given that a score of 1 corresponds to complete reproductive isolation, this number indicates strong reproductive isolation.
Three Points of Critique
A few months later, David Toews and his colleagues published a critique on this conclusion of strong reproductive isolation, raising three main issues. First, the plumage classification scheme in the original study is not suitable to determine hybrid ancestry in these warblers. Recent genetic work by Marcella Baiz and her colleagues showed that none of the six “Brewster’s Warblers” that they analyzed were first-generation hybrids (see this blog post for the details). Moreover, many warblers that look like pure phenotypes might actually contain some genetic ancestry from past hybridization. The original study did not take these “cryptic hybrids” into account.
A second issue that was not considered in the analyses concerns extra-pair copulations in which birds mate with other individuals besides their social partner. This phenomenon has been well-documented in Vermivora warblers and could significantly contribute to hybridization between Golden-winged and Blue-winged Warblers.
Finally, Toews et al. (2021) pointed out that behavioral isolation is not always sufficient to maintain complete reproductive isolation. For example, recent simulations by Darren Irwin showed that assortative mating on its own cannot prevent populations from merging, some form of postzygotic isolation is needed (see this blog post for the whole story). Although “Brewster’s Warblers” have lower pairing success compared to pure phenotypes, their reproductive output might still be too high to prevent genetic exchange. Hence, the authors of the critique argue that “extensive mixing in areas of sympatry is more consistent with low levels of total reproductive isolation—that is, both low pre-and postmating isolation—and results in high gene flow.”
Recently, the authors of the original study – this time led by Cody Porter – replied to the critique by Toews et al. (2021). First, with regard to the unsuitability of the plumage classification scheme, they explain that the complex genetic ancestry of the warblers (including cryptic hybrids) is actually not that relevant for their question. The focus of their study concerns different plumage phenotypes, not the whole genomic context. They write: “In essence, our study could be viewed as testing whether the six major genomic differences between V. chrysoptera and V. cyanoptera (which largely correspond to plumage differences; Toews et al., 2016) promote reproductive isolation.”
Second, they argue that extra-pair copulations were unlikely to bias their results, referring to the findings of Vallender et al. (2007). This study found only 3 cases of extra-pair copulations (ca. 1.5%) between different phenotypes. In two cases a hybrid female mated with a Golden-winged Warbler and in one case a Golden-winged Warbler female mated with a hybrid.
The third point of critique focuses on the contribution of behavioral isolation to the level of reproductive isolation. You need some degree of postzygotic isolation to prevent species from merging. Toews et al. (2021) argued that the reproductive success of the hybrids is still too high, facilitating gene flow between the species. The authors counter this argument by highlighting the 26% reduction in the pairing success of phenotypic hybrids compared to both parental forms and the fact that only 1.2% of birds with a “pure” phenotype paired with an individual of the alternative phenotype. These numbers “appear to fall well within the parameters for a stable hybrid zone according to Irwin’s (2020) simulations.”
You might be wondering who won this debate? I don’t think this is the right question to ask here. Both groups of authors approached the scientific conundrum of reproductive isolation from a different perspective. The original study focused on behavioral isolation on the phenotypic level, whereas the critique used the genomic patterns of introgression as a starting point. At first sight, the strong reproductive isolation between plumage phenotypes seems incompatible with the largely homogeneous genomes of these warblers. However, reproductive isolation is not complete (remember the score of 0.96), which seems to allow for enough gene flow to homogenize the majority of the genome. Only the genomic regions containing “plumage genes” are able to withstand this homogenizing force.
Similar patterns have been described in other avian systems, such as Hooded Crow (Corvus cornix) and Carion Crow (C. corone) or Taiga Bean Goose (Anser fabalis) and Tundra Bean Goose (A. serrirostris). A few divergent genomic regions seem to be sufficient for a high level of reproductive isolation. We need more studies that quantify reproductive isolation at the phenotypic level and provide a link with the genomic underpinnings of the isolation barriers. Studying the evolution of reproductive isolation from different perspectives – behavioral, morphological and genetic – will fuel healthy debates and will provide more insights into the origin of species.
Confer, J. L., Porter, C., Aldinger, K. R., Canterbury, R. A., Larkin, J. L., & Mcneil Jr, D. J. (2020). Implications for evolutionary trends from the pairing frequencies among golden‐winged and blue‐winged warblers and their hybrids. Ecology and Evolution, 10(19), 10633-10644.
Toews, D. P., Baiz, M. D., Kramer, G. R., Lovette, I. J., Streby, H. M., & Taylor, S. A. (2021). Extensive historical and contemporary hybridization suggests premating isolation in Vermivora warblers is not strong: A reply to Confer et al. Ecology and Evolution.
Porter, C. K., Confer, J. L., Aldinger, K. R., Canterbury, R. A., Larkin, J. L., & McNeil Jr, D. J. (2021) Strong yet incomplete reproductive isolation in Vermivora is not contradicted by other lines of evidence: A reply to Toews et al. Ecology and Evolution.
Featured image: Golden-winged warbler (Vermivora chrysoptera) © Bettina Arrigoni | Wikimedia Commons
These papers have been added to the Parulidae page.