Genetic analyses uncover several hybrids and backcrosses in France.
In 2013, French researchers discovered a mixed pair of Common Swift (Apus apus) and Pallid Swift (Apus pallidus). This observation raised the question how common hybridization is between these two species. Identifying hybrids based on morphological traits is extremely challenging. Indeed, even “pure” Common and Pallid Swifts are difficult to tell apart. That is why Alice Cibois and her colleagues turned to genetic data. They inspected the genetic make-up of almost 500 individuals.
The sampling effort centered around the French town of Bastia (Corsica) where both species are breeding. The researchers noted that “although the two species are known to form mixed colonies at the same natural sites, sympatry predominantly occurs within urban regions where both species breed in buildings.” The chances of finding hybrids are thus highest in these urban areas.
Recent Hybrids and Backcrosses
The mitochondrial gene COI provided the first clue for hybridization. A haplotype network uncovered six Pallid Swift individuals with mitochondrial sequences of the Common Swift. Nuclear markers – a set of nine microsatellites – provided more detailed patterns of hybridization. The analyses suggested four first-generation hybrids and ten backcrosses (indicating that the hybrids are fertile). These findings highlight the power of genetic data to document hybridization between morphologically similar species. The researchers nicely address this topic in the discussion of their paper:
Observers never reported a mixture of phenotypic traits suggestive of a hybrid origin. Genotyping at nuclear markers is thus the only tool available to reliably identify individuals with hybrid origin and to track the dynamics of introgression between the two species.
Haplotype network for Common Swifts (blue) and Pallid Swifts (orange). The circles are proportional to the number of individuals. Asterisks show the six individuals identified as Pallid Swifts that have Common Swift haplotypes. From: Cibois et al. (2022).
Anthropogenic Hybridization
As expected, most of these admixed individuals were found in and around the city of Bastia. This pattern supports the idea that human actions can lead to hybridization. And it is not just limited to swifts. In a previous blog post, for example, I explained how nectar feeders and ornamental plants in gardens might have facilitated hybridization between two subspecies of Allen’s Hummingbird (Selasphorus sasin). Similarly, another recent study reported that hybrids between four species of chickadee (genus Poecile) were more common in urban settings (see this blog post). Urbanization might thus fuel hybridization.
References
Cibois, A., Beaud, M., Foletti, F., Gory, G., Jacob, G., Legrand, N., … & Thibault, J. C. (2022). Cryptic hybridization between Common (Apus apus) and Pallid (A. pallidus) Swifts. Ibis, 164(4), 981-997.
The comparison of three species pairs leads to some surprising findings.
In 2005, Thomas Turner and his colleagues reported on “genomic speciation islands” in the African malaria mosquito (Anopheles gambiae). In their PLoS Biology paper, the authors described how some genomic regions remain differentiated despite considerable gene flow, and they speculated that these regions might contain the genes responsible for reproductive isolation. However, further studies on other organisms, such as Heliconius butterflies and Ficedula flycatchers, indicated that the term “speciation islands” was a bit premature. Other evolutionary processes can give rise to differentiated genomic islands. To understand how these genomic islands can arise, we must first take a closer look at the popular summary statistic Fst.
The fixation index (Fst) is a measure of population differentiation due to genetic structure. It is important to realize that Fst is a relative measure because it compares the genetic diversity between populations while taking into account the genetic diversity within each population (you can nicely see this in the formula below, where π is genetic diversity). Hence, you can get a peak in Fst at a certain genomic region when one population has low genetic diversity at this location. This reduction in genetic diversity can be the outcome of genetic drift or a selective sweep, and might thus be unrelated to reproductive isolation. This issue with Fst can be resolved by calculating another summary statistic (Dxy) which is not influenced by genetic diversity within populations. The relationship between Fst and Dxy can be very insightful: Fst peaks that result from locally reduced gene flow are predicted to have elevated Dxy, while Fst peaks resulting from lower genetic diversity in a population are not.
One way to calculate Fst which nicely shows the effect of genetic diversity within a population.
Hummingbirds and Chromosomes
With this knowledge in mind, evolutionary biologists try to understand how genetic differentiation accumulates in the genome during speciation. Are peaks in Fst related to reproductive isolation or are they the outcome of reduced genetic diversity? Because it is mostly not feasible to document the entire speciation process (which takes at least thousands of years), researchers compare closely related species pairs at different stages of divergence. A recent study in the journal BMC Evolutionary Biology focused on three pairs of hummingbirds that diverged at different times, namely:
Anna’s (Calypte anna) and Costa’s hummingbird (C. costae) – 2.5 million years
Black-chinned (Archilochus alexandri) and Ruby-throated hummingbird (A. colubris) – 1.5 million years
Allen’s (Selasphorus sasin) and Rufous hummingbirds (S. rufus) – 0.93 million years
The researchers – Elisa Henderson and Alan Brelsford – were mainly interested in the role of recombination in the build-up of genetic differentiation. Low recombination rates are predicted to lead to reduced genetic diversity because selection on one genetic variant will affect large genomic regions that are linked to this variant. If recombination rate is high, however, the genetic variant under selection will be confined to a smaller genomic region and the reduction in genetic diversity will be more localized. Given that large chromosomes have lower recombination rates, we can expect bigger reductions in genetic diversity and consequently more peaks in Fst. In other words, larger chromosomes will diverge faster compared to smaller chromosomes. In addition, sex chromosomes (Z and W for birds) also show reduced recombination and can thus accumulate genetic differentiation faster than autosomes.
The genomic landscape of differentiation for three pairs of hummingbird species. From: Henderson & Brelsford (2020) BMC Evolutionary Biology.
Fast Microchromosomes
The genomic analyses resulted in some interesting results. The authors found that “speciation seems to progress at different rates based on chromosome type, with the sex chromosome diverging first, the microchromosomes diverging next, and divergence only appearing on the macrochromosomes in late stages of reproductive isolation.” The finding that sex chromosomes diverge first is logical. These chromosomes show reduced rates of recombination and are known to accumulate incompatible alleles that can contribute to reproductive isolation (see for example this blog post on the Reunion grey white-eye, Zosterops borbonicus).
Given the predictions outlined above, the result that microchromosomes diverge before macrochromosomes is quite surprising. Given the lower recombination rate on larger chromosomes, we would have expected the opposite pattern. The authors suspect that the early accumulation of Fst peaks on microchromosomes may be due to certain characteristics of these small chromosomes. For example, microchromosomes have a high gene density which might provide more targets for selection, leading to lower genetic diversity and consequently peaks in Fst. Or perhaps these small chromosomes might harbor specific genes that contribute to reproductive isolation? More research is needed to pinpoint the exact mechanisms.
Genomic analyses showed that genetic differentiation (measured as Fst) accumulated faster on sex chromosomes (red), followed by microchromosomes (blue) and macrochromosomes (purple). From: Henderson & Brelsford (2020) BMC Evolutionary Biology.
Barrier Loci?
Apart from Fst, the researchers also calculated Dxy. As explained above, Fst peaks that result from locally reduced gene flow are predicted to have elevated Dxy, while Fst peaks resulting from lower genetic diversity in a population are not. In this case, there was a negative correlation between Fst and Dxy, suggesting that most differentiated regions are the outcome of lower genetic diversity in one population (due to genetic drift or selection). There might be some genomic regions that are involved in reproductive isolation, but more detailed analyses are needed to find these.
This study shows how we can gain insights into the process of speciation by comparing species pairs at different stages of divergence. There is, however, an important issue to take into account when performing these kinds of analyses. Namely, species-specific differences in natural history and morphology can lead to different genetic signatures during the speciation process. The authors nicely formulated this caveat at the end of their paper.
These differences across the species used in this study highlight that each species pair is subject to its own evolutionary trajectory leading to a unique speciation event. While this is a general caveat of using independent species pairs as a proxy for the speciation continuum, we believe that the differences we observe among chromosome types can inform the ongoing debate about the roles of selection and recombination in the genetics of speciation.
References
Henderson, E. C., & Brelsford, A. (2020). Genomic differentiation across the speciation continuum in three hummingbird species pairs. BMC Evolutionary Biology, 20(1), 1-11.
Genetic analyses uncover a hybrid population in southern California.
In 1966, ornithologists recorded breeding Allen’s Hummingbirds (Selasphorus sasin) on the Palos Verdes Peninsula in Los Angeles County (California). Morphological measurements and analyses of ringing data suggested that these hummingbirds belong to the subspecies sedentarius, which can be found on the Channel Islands in southern California. The move to the mainland might have been facilitated by human activities, such as nectar feeders and ornamental plants in gardens. However, a recent study in the journal Conservation Genetics shows that the situation is more complex than the population expansion of one subspecies.
Three Clusters
Between 2004 and 2016, Braden Godwin and his colleagues collected samples from Allen’s Hummingbirds across California. Genetic analyses revealed three main clusters: the northern California mainland, the Channel Islands and the newly established urban population. The northern cluster contains members of the migratory species sasin, whereas the Channel Islands cluster corresponds to the sedentary subspecies sedentarius. But what about the urban population? It is clearly a separate genetic cluster (see figure below), but does it contain sedentarius individuals as suggested by previous studies?
The answer is not a straightforward yes or no. The population has genetic signatures from sedentarius, but also from the other subspecies. In other words, it is a hybrid population. Indeed, the researchers conclude that “our population genomic analyses indicate that S. sasin hummingbirds inhabiting mainland southern California are a hybrid population resulting from admixture between S. s. sasin and S. s. sedentarius.”
A principal component analysis reveals three genetic clusters that correspond to northern California (NC), the Channel Islands (CI) and the newly established urban population (SC). The latter one turned our to be a hybrid population. From Godwin et al. (2020) Conservation Genetics
Good or bad?
The formation of this hybrid population is a nice example of human-induced hybridization. The nectar feeders and ornamental flowers in Californian gardens attract hummingbirds from different subspecies that consequently interbreed. A few months ago, I published a review paper on this topic in the journal Evolutionary Applications. In that study I touched upon the benefits and dangers of human-induced hybridization: “While the interbreeding of different populations or species can have detrimental effects, such as genetic extinction, it can be beneficial in terms of adaptive introgression or an increase in genetic diversity.” From a conservation point of view, we are thus faced with a difficult dilemma: should we prevent potential genetic extinction with conservation measures (e.g., culling hybrids) or should we not intervene to provide the opportunity for adaptive introgression and an increase in genetic diversity?
The same question applies to the hummingbird situation. And although the authors mention the issues of genetic swamping and extinction, they focus on the positive side of this hybridization event.
The southern California hybrid zone could act as a conservation reservoir for S. s. sasin alleles in the face of potentially declining abundance and potential maladaptive alleles introduced by S. rufus [i.e. rufous hummingbird] or as a beneficial introduction of new alleles from S. s. sedentarius to potentially help the declining S. s. sasin subspecies. The expanding population of Allen’s Hummingbirds in southern California could be interpreted as a positive development as the overall population of the species appears to be increasing and alleles specific to S. s. sasin are remaining in the subspecies complex
Hybridization is not always bad news for conservation.
References
Godwin, B. L., LaCava, M. E., Mendelsohn, B., Gagne, R. B., Gustafson, K. D., Stowell, S. M. L., Engilis Jr., A., Tell, L. A. & Ernest, H. B. (2020). Novel hybrid finds a peri-urban niche: Allen’s Hummingbirds in southern California. Conservation Genetics, 21(6), 989-998.
Avian Hybrids 