Reclassifying Robins: Two new species on the Canary Islands

Multiple lines of evidence point to distinct species on Tenerife and Gran Canaria.

The European Robin (Erithacus rubecula) is inextricably linked to Christmas in many European countries. The origin of this association is unclear, but several explanations have been proposed. One possible reason, for example, concerns postmen in Victorian Britain. These postmen were known as “robins” because of their red-breasted uniforms. Artists usually illustrated Christmas cards with scenes related to the delivery of letters, such the red-breasted postmen. At some point, the artists started to draw the familiar little brown bird delivering letters instead of the postmen. Other explanations go back earlier in time and provide direct links with Christianity (see this article for several stories). Whatever the reason for Robin on your Christmas card, it seems like the perfect time to delve into the taxonomy of this small passerine.

The European Robin is widely distributed – from western Siberia to the Macaronesian Islands – and shows considerable geographic variation, leading to the recognition of eight subspecies. A recent study in the journal Zoologica Scripta took at closer look at two subspecies on the Canary Islands (E. r. superbus on Tenerife and E. r. marionae on Gran Canaria). Based on genetics, song and plumage patterns, the researchers argued to elevate these subspecies to the species level.

Gathering Evidence

The study took an integrative approach to taxonomy, combining several lines of evidence to support the species status of the taxa. Let’s start with the genetic data. Phylogenetic analyses of the mitochondrial gene cytb uncovered three distinct lineages, representing birds from Europe (rubecula-lineage), Tenerife (superbus-lineage) and Gran Canaria (marionae-lineage). These three lineages showed substantial genetic divergence of more than 4%. This is well above the species-level threshold of 2% that is used for DNA-barcoding studies on birds (but see this blog post for the unreliability of only relying on these barcodes). Moreover, the researchers found no shared haplotypes among the lineages, suggesting that there is not gene flow between them (although this remains to be confirmed with nuclear data).

Next, the researchers compared 1413 songs of 60 individuals. These analyses uncovered numerous vocal differences – too many to list here – among the three genetic lineages. A discriminant function analysis (DFA) based on 24 song variables nicely separated the birds into three distinct clusters. Clearly, Robins from Europe, Tenerife and Gran Canaria sing different songs.

Finally, the birds from the Canary Islands (E. r. superbus and E. r. marionae) differ from their European counterparts in several plumage traits: (1) the presence of a pale eye ring, (2) a darker and greyer band of ash-grey on forecrown and from side of crown down to side of breast, (3) deeper rufous-chestnut face and chest, (4) darker, greyish olive upperparts, and (5) whiter belly and vent.

Analyses based on genetic data (left) and vocalizations (right) supported the recognition of three distinct Robin species.

Evolutionary History

As shown above, all lines of evidence converge upon the decision to split the European Robin into three species: E. rubecula, E. superbus and E. marionae. Apart from this taxonomic rearrangements, this study also reveals an interesting observation. At the end of the discussion, the researchers remark that:

The pattern of phylogenetic relationships of robins suggests that the colonisation of the extant robins in the Canary Islands was not the result of one wave but two or three.

Understanding how the European Robin colonized these islands is an exciting question to explore. And we don’t need a Christmas miracle to explain it. Just some solid science.

References

Sangster, G., Luksenburg, J. A., Päckert, M., Roselaar, C. S., Irestedt, M., & Ericson, P. G. (2022). Integrative taxonomy documents two additional cryptic Erithacus species on the Canary Islands (Aves). Zoologica Scripta, 51(6), 629-642.

Featured image: European Robin (Erithacus rubecula) © Francis C. Franklin | Wikimedia Commons

The beak color of the finch

Why do some nestlings in Darwin’s Finches have a yellow beak?

When I write the following sequence – AA, Aa, and aa – you might immediately think of Mendelian genetics. In high school, countless students have learned how to determine the genetic basis of a particular trait from the combination of dominant (A) and recessive (a) genetic variants or alleles. A popular example, apart from Mendel’s peas, concerns eye color: the brown allele is dominant while blue one is recessive. Put the parental combinations in a Punnett square and you can deduce the eye color of their offspring. The reality, however, is more complicated. In humans, eye color is determined by at least 16 genes. Simple Mendelian traits with one dominant and one recessive allele seem to be quite rare. Most traits are polygenic (i.e. influenced by many genes). But from time to time, researchers stumble upon a classic Mendelian case, such as the beak color of nestlings in Darwin’s Finches.

One Gene

In a recent Current Biology study, Erik Enbody and his colleagues unraveled the genetic basis of beak color in young Darwin’s Finches. Previous work showed that nestlings have either pink or yellow beaks. Tracing this trait across a pedigree revealed that it follows basic Mendelian rules: the yellow phenotype is recessive while the pink one is dominant.

Using genomic data for the Common Cactus Finch (Geospiza scandens) and the Medium Ground Finch (Geospiza fortis), the researchers could trace the genetic basis of this trait to a region on chromosome 24. Close inspection of this genomic region pointed to a single nucleotide variant in the gene BCO2. The exact mechanism associated with this genetic variant remains unknown, but might be related to differential gene expression. A less active BCO2-gene results in the deposition of more carotenoid pigments, culminating in a yellow beak.

Nestlings of Darwin’s Finches have either a yellow or a pink beak (Figure A). Genetic analyses of Medium Ground Finch and Common Cactus Finch converged upon the gene BCO2, which resides on chromosome 24 (Figures B and C). A single variant in this gene determines the beak color (Figures D and E). Lower expression of the recessive yellow allele probably results in the yellow phenotype (Figure F). From: Enbody et al. (2021).

Carotenoid Advantages

The different beak color is not restricted to nestlings of the Medium Ground Finch and the Common Cactus Finch. Numerous other species in the Darwin’s Finches radiation show these phenotypes. Plotting this trait on a phylogenetic tree suggests that it arose roughly 0.5 million years ago when the Vegetarian Finch (Platyspiza crassirostris) lineage split from the ground and tree finches. This pattern raises an intriguing question: how was the variation in beak morphology maintained in all these species?

The researchers explored several options. Perhaps heterozygous individuals do better than homozygous ones, ensuring that the recessive allele continues to circulate in the population. There was, however, no evidence for such a heterozygote advantage in the studies species. Or maybe the yellow beak color triggers the parents to bring more food to the nest. This signaling effect sounds plausible, but it is not supported by observations of parental feeding.

In the end, the researchers speculated about possible advantages of increased carotenoid pigments in the yellow beaks of nestlings. First, collecting these pigments in the beak might protect the birds from accumulating toxic products in their body when the carotenoids are broken down. Second, the yellow phenotype could influence maternal investment. Chickens with the yellow skin phenotype (also related to the BCO2-gene) invest more carotenoids in the egg yolk. The same could occur in Darwin’s Finches. Third, variation in carotenoids might alter the color perception of the avian retina (known as spectral tuning) with possible fitness consequences. Plenty of hypotheses to explore, but finding the correct explanation will not be as easy as shelling peas.

The frequency of the yellow allele across the Darwin’s finch radiation. The yellow stars indicate species with the yellow allele, while the black stars point to species without it. The big yellow star corresponds to the likely origin of the allele. From: Enbody et al. (2021).

References

Enbody, E. D., Sprehn, C. G., Abzhanov, A., Bi, H., Dobreva, M. P., Osborne, O. G., Ruben, C.-J., Grant, P.R., Grant, B.R. & Andersson, L. (2021). A multispecies BCO2 beak color polymorphism in the Darwin’s finch radiation. Current Biology, 31(24), 5597-5604.

Featured image: Common Cactus Finch (Geospiza scandens) © Mike’s Birds | Wikimedia Commons

The evolution of multi-copy genes on the W-chromosome

Is this avian sex-chromosome comparable to the mammalian Y-chromosome?

The Y-chromosome looks pretty pathetic in comparison with the much bigger X-chromosomes. In mammals, this male sex-chromosome went its separate evolutionary way when it acquired a sex-determining gene and stopped recombining with other chromosomes. The result is a decaying chromosome that harbors few functional genes. Interestingly, many of these remaining genes have experienced massive amplification, resulting in several multi-copy gene families. The exact trigger for this increase in gene copy numbers remains a matter of debate, but could be related to strong selection in males for sperm competition. More expressed Y-linked genes might improve sperm mobility (see for example this study).

The study of multi-copy genes on sex-chromosomes has mainly focused on the Y-chromosome (in mammals and Drosophila). What about the W-chromosome in birds? This small sex-chromosome is female-specific and not susceptible to sperm competition. We might thus expect different evolutionary dynamics on the W-chromosome. That is why Thea Rogers and her colleagues decided to take a closer look at multi-copy genes on this chromosome. Is it comparable to or drastically different from the Y-chromosome?

Counting Genes

The researchers quantified the variation in copy number of 26 W-linked genes in several duck breeds. Using a special molecular technique – NanoString nCounter assay – they found that most of these genes were present in single copies. Only the genes HINTW (18 copies) and KCMF1W (2 or 3 copies) have undergone amplification in ducks. This pattern contrasts with the situation on the Y-chromosome where massive gene amplification took place. What could explain the difference between these chromosomes?

The researchers offer several possibilities, such as the role of genetic drift and meiotic drive dynamics. In this blog post, however, I would like to focus on the explanation I introduced above: sperm competition. The W-chromosome is not affected by this competition where multiple gene copies might improve sperm success. Because there is no similar selection pressure on female fertility, having multiple versions of the same gene is not a suitable strategy. There is, however, an exception: the gene HINTW.

Variation in copy number for the gene HINTW in duck breeds (A) and chicken breeds (B). These patterns suggest selection for female fertility in the chicken breeds.

Egg Production

As mentioned in the previous section, the gene HINTW has 18 copies in the duck breeds. In chicken breeds, however, we observe some striking variation, ranging from 7 copies in the wild Red Junglefowl to 17 copies in the Black Minorca breed. Interestingly, the number of gene copies seems to be related to selection for egg production:

We find a general trend that breeds which have been selected for egg production via artificial female-specific selection, had on the average higher number of copies relative to breeds that have been bred for male fighting and plumage and subject to relaxed female-specific selection.

So, similar to the effects of male sperm competition on the Y-chromosome, artificial selection for female egg production can impact the number of gene copies on the W-chromosome. These sex-chromosomes might not be that different after all.

References

Rogers, T. F., Pizzari, T., & Wright, A. E. (2021). Multi-copy gene family evolution on the avian W chromosome. Journal of Heredity, 112(3), 250-259.

Featured image: Runner ducks © Bjoern Clauss | Wikimedia Commons

Calling fast and slow: Hybridization risk affects female choice in Spadefoot Toads

The presence of another species changes female preferences.

From an evolutionary perspective, individuals “want” to get their genes into the next generation, and beyond. Finding a suitable partner is thus of utmost importance. Mating with a different species is a tricky strategy that can be successful, as illustrated by cases of adaptive introgression (see for example this blog post). In most cases, however, hybridization will be detrimental. The resulting hybrid offspring can be unviable or sterile, sending an individuals genes into an evolutionary dead-end.

The risk of maladaptive hybridization could act as a selective force, potentially shaping the evolution of certain behaviors. Take, for example, Mexican Spadefoot Toads (Spea multiplicata). Females of this species tend to prefer males with fast calling rates, because a rapid fire of calls signals a good condition. However, a closely related species – the Plains Spadefoot Toad (Spea bombifrons) – also produces fast calls. Females of the Mexican species might mistake males of the Plains Spadefoot Toad for potential partners, which might lead to maladaptive hybridization. Selection against hybridization would favor Mexican females that prefer slower calling males of their own species.

Choice Experiment

Gina Calabrese and Karin Pfennig put this idea to the test. They collected 53 females of the Mexican Spadefoot Toad and subjected them to a choice experiment. The toads were exposed to two speakers: one with a fast calling rate (37 calls per minute) and one with a slow calling rate (26 calls per minute). Meanwhile, the researchers played a background chorus of calling toads. This chorus consisted of either only Mexican Spadefoot Toads or a mixture of Mexican and Plains Spadefoot Toads. This clever experimental set-up allowed the researchers to see whether female toads will adjust their preference – by hopping to one of the speakers – when hybridization with another species is a possibility.

At the beginning of the results section, we find a good summary of the findings: “Female preferences depended on the presence of heterospecifics in the chorus background. In the mixed-chorus background, females preferred the slower call rate. In the pure-conspecific chorus treatment, however, females as a group did not express a preference.” So, indeed, female Mexican Spadefoot Toads change their preference for calling males if they run the risk of hybridizing.

The choice experiment revealed that females show no preference when only one species is calling in the background (left section). When a mixed chorus is playing, however, the females mainly select slow-calling males (right section). From: Calabrese & Pfennig (2022).

Sexual Selection

The outcomes of this experiment suggest that female choice – and thus sexual selection – can change when the risk of maladaptive hybridization is high. Although this study focuses on amphibians, I cannot help but extend this insight to birds. It is easy to imagine that similar situations can occur in our feathery friends. And indeed: in a 1997 Nature paper, Glenn-Peter Saetre (who I actually met a few months ago, see this blog post) and his colleagues reported that female Pied Flycatchers (Ficedula hypoleuca) prefer dull males when Collared Flycatchers (F. albicollis) are around. Normally, females of this species select high-quality black-and-white males. But the risk of maladaptive hybridization – hybrids are sterile – forces females to change their preferences. Mate choice is not an easy process…

References

Calabrese, G. M., & Pfennig, K. S. (2022). Females alter their mate preferences depending on hybridization risk. Biology Letters, 18(11), 20220310.

Saetre, G. P., Moum, T., Bureš, S., Král, M., Adamjan, M., & Moreno, J. (1997). A sexually selected character displacement in flycatchers reinforces premating isolation. Nature, 387(6633), 589-592.

Featured image: Mexican Spadefoot Toad (Spea multiplicata) © William L. Farr | Wikimedia Commons