A genetic test of the theory of island biogeography using the Fiji bush-warbler

Do patterns of gene flow follow the predictions of this classic theory?

Islands biology was one of my favorite courses during my Master at the University of Antwerp (Belgium). Not only did we travel to a collection of small islands of the coast of Croatia, we delved into the details of the evolution and ecology of island species. I still remember sitting outside while reading “The Theory of Island Biogeography“, a classic textbook by Robert H. MacArthur and E.O. Wilson (published in 1967). This books contains an iconic graph where they mathematically show how the number of species on an island is the equilibrium between colonization and extinction, taking into account the size and location of the island. Numerous ecologists have tested the predictions that came out of this simple mathematical model, resulting in several revisions of the theory of island biogeography (see for example this book by Jonathan Losos and Robert Ricklefs).

The rapid developments in genomic sequencing now allow scientist to test some classic predictions from a genetic point of view. For example, patterns of gene flow are expected to be influenced by the size and location of the island. A larger island can send out more migrants to smaller islands, so genes will probably flow from larger to smaller islands. In addition, remote islands are difficult to reach and will probably receive less migrants. Hence, gene flow will be negative correlated with distance between the islands. A recent study in the journal Molecular Ecology tested these straightforward predictions in Fiji, an isolated archipelago in the southwest Pacific.

A classic graph from “The Theory of Island Biogeography”, showing that the number of species on an island is the equilibrium between colonization and extinction. From: Geography Realm.

Demographic Analyses

Fiji is composed of four main islands (Taveuni, Vanua Levu, Viti Levu, and Kadavu), surrounded by hundreds of smaller islands. Ethan Gyllenhaal and his colleagues focused on a songbird that is endemic to the four large islands: the Fiji bush-warbler (Horornis ruficapilla). Using ultraconserved elements, the researchers mapped the genetic population structure of this island bird and estimated the levels of gene flow between the different islands. They nicely summarized their results in the abstract: “Our demographic analysis inferred low levels of gene flow from each large island to its small counterpart and little or none in the opposite direction. The difference in the distance between these two island pairs manifested itself in lower levels of gene flow between more distant islands.” These findings are in line with the predictions that we outlined above.

An unexpected finding was that the number of migrants from Viti to Vanua Levu was much smaller than that of Viti Levu to Kadavu even though Vanua Levu is closer (76 versus. 62 km) and acts as a larger target. This pattern does not follow the predictions of the theory of island biogegraphy and might require additional explanation. The researchers offer several possible mechanisms. First, the prevailing winds in Fiji are easterlies which would hamper the westward dispersal from Viti Levu to Vanua Levu. A similar pattern has been documented in penguins where gene flow follows the ocean currents between populations (see this blog post for the whole story). Second, there might be some degree of reproductive isolation between the island populations. Previous work reported that southern populations have more complex songs than their northern relatives, which could act as a reproductive barrier. Or there might even be some genetic differences that lead to lower fitness in inter-island hybrids. More research is needed to solve this mystery, perhaps leading to another refinement of the theory of island biogeography.

Patterns of gene flow between different island populations based on demographic analyses of ultraconserved elements. The arrows depict the presence and relative strength of gene flow. From: Gyllenhaal et al. (2020) Molecular Ecology.


Gyllenhaal, E. F., Mapel, X. M., Naikatini, A., Moyle, R. G., & Andersen, M. J. (2020). A test of island biogeographic theory applied to estimates of gene flow in a Fijian bird is largely consistent with neutral expectations. Molecular Ecology29(21), 4059-4073.

Featured image: Fiji bush-warbler (Horornis ruficapilla) © Lars Petersson | Oiseaux.net

This paper has been added to the Cettiidae page.

Exploring the speciation continuum of hummingbirds

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.


Henderson, E. C., & Brelsford, A. (2020). Genomic differentiation across the speciation continuum in three hummingbird species pairs. BMC Evolutionary Biology20(1), 1-11.

Featured image: Ruby-throated hummingbird (A. colubris) © JeffreyW | Wikimedia Commons

The paper has been added to the Apodiformes page.

You only need one genome to unravel the demographic history of the Chinese Grouse

Genomic analyses reveal population fluctuations during the Pleistocene.

A few weeks ago, scientists announced that they almost completed a sequence of the human genome. This might come as a surprise: did we not sequence the human genome in 2003 when the results from the Human Genome Project were published? That genome sequence was actually incomplete, about 15% was missing (especially stretches of repetitive DNA are difficult to assemble). Similarly, many avian genome assemblies contain significant gaps (see this blog post for more details). However, scientists can still extract a lot of information from incomplete genome assemblies. For instance, you can reconstruct the demographic history of a species from one genome using a pairwise sequentially Markovian coalescent (PSMC) analysis. This technique – developed by Heng Li and Richard Durbin – is nicely explained by David Reich in his book Who We Are and How We Got Here:

A 2011 paper by Heng Li and Richard Durbin showed that the idea that a single person’s genome contains information about a multitude of ancestors was not just a theoretical possibility, but a reality. To decipher the deep history of a population from a single person’s DNA, Li and Durbin leveraged the fact that any single person actually carries not one but two genomes: one from his or her father and one from his or her mother. Thus it is possible to count the number of mutations separating the genome a person receives from his or her mother and the genome the person receives from his or her father to determine when they shared a common ancestor at each location. By examining the range of dates when these ancestors lived—plotting the ages of one hundred thousand Adams and Eves—Li and Durbin established the size of the ancestral population at different times. In a small population, there is a substantial chance that two randomly chosen genome sequences derive from the same parent genome sequence, because the individuals who carry them share a parent. However, in a large population the chance is far lower. Thus, the times in the past when the population size was low can be identified based on the periods in the past when a disproportionate fraction of lineages have evidence of sharing common ancestors.

Population Fluctuations

A recent study in the journal BMC Genomics applied this PSMC analysis to the genome of a Chinese Grouse (Tetrastes sewerzowi). This forest-dwelling species can be found in the mountains east of the Qinghai-Tibet Plateau. It is currently considered “Near Threatened” because of population declines due to ongoing deforestation and fragmentation of its habitat.

The genomic analyses revealed that the population size of the Chinese Grouse has fluctuated over time. Populations decreased during early to middle Pleistocene but showed an expansion during late Pleistocene (between 30,000 and 40,000 years ago), followed by a sharp decline during the last glacial maximum (about 20,000 years ago). Similar patterns have been found in other bird species, highlighting the influence of the climatic cycles during the Pleistocene (see for example this study by Krystyna Nadachowska-Brzyska and her colleagues).

The PSMC analysis showed population fluctuations of the Chinese Grouse during the Pleistocene. From: Song et al. (2020) BMC Biology.

Coniferous Forests

Next, the researchers focused on the underlying mechanisms of these population fluctuations. Why did the number of Chinese Grouse wax and wane during the Pleistocene? To answer this question, the researchers turned to Ecological Niche Modelling and reconstructed the distribution of the Chinese Grouse throughout the Pleistocene. This exercise showed that the population expansion during the late Pleistocene (30,000–40,000 years ago, also known as the Greatest Lake Period) can be explained by the warmer weather which allowed conifer forests, the primary habitat for Chinese Grouse, to reach their greatest extent. Later on, during colder periods, the coniferous habitat shrunk and the Chinese Grouse populations moved westwards into higher altitudes.

These findings indicate that the distribution of the Chinese Grouse is strongly dependent on the coniferous forest cover. It is thus essential to protect these fragmented forests and safeguard the future of this beautiful bird.

Ecological Niche Modelling showed how the suitable habitat for Chinese Grouse increased during the late Pleistocene (figure a), followed by extensive loss of habitat later on (figure b). The current distribution is depicted in figure c. From: Song et al. (2020) BMC Genomics.


Song, K., Gao, B., Halvarsson, P., Fang, Y., Jiang, Y. X., Sun, Y. H., & Höglund, J. (2020). Genomic analysis of demographic history and ecological niche modeling in the endangered Chinese Grouse Tetrastes sewerzowiBMC genomics21(1), 1-9.

Featured image: A drawing of Chinese Grouse (Tetrastes sewerzowi) © Ornithological Miscellany. Volume 2 | Wikimedia Commons

How many rosy-finch species are there in North America?

Phylogenomic analyses try to solve this taxonomic puzzle.

Ornithologists have created several world bird lists to summarize avian taxonomy, such as the International Ornithological Community (IOC) World Bird List or the Howard and Moore Checklist. These checklists do not always agree on the classification of specific birds (see for example this study on raptors), leading to heated debates between taxonomists. Take, for instance, the rosy-finches of the genus Leucosticte in North America. The American Ornithologists’ Union recognizes three species: the gray-crowned rosy-finch (L. tephrocotis), the brown-capped rosy-finch (L. australis), and the black rosy-finch (L. atrata). In the Howard and Moore checklist, however, they are lumped into one species.

The lumped arrangement is based on a 2009 study in Molecular Phylogenetics and Evolution where Sergei Drovetski and his colleagues could not discriminate between the three American taxa using the mitochondrial gene ND2 and two autosomal genes. They attributed the lack of genetic differentiation to gene flow between neighboring populations. However, can we base a taxonomic decision on a handful of genes? These taxa clearly look distinct. Perhaps these morphological differences can be traced back to a few genomic regions, similar to golden-winged warbler (Vermivora chrysoptera) and blue-winged warbler (V. pinus) where a few “plumage genes” are responsible for their distinct plumage patterns. To test this idea, Erik Funk and his colleagues used genomic data to study the evolution of the rosy-finches in North America. Their findings recently appeared in the journal Systematic Biology.

Three Species?

Using whole genome sequencing data from 68 individuals, the researchers reconstructed the phylogenetic relationships between the different taxa. The analyses provided support for three American species: the black rosy-finch, the brown-capped rosy-finch, and the Alaska island rosy-finch. The first two are already considered distinct species by the AOU, while the populations on the Alaskan islands are currently classified as two subspecies within the grey-crowned rosy-finch (griseonucha and umbrina). The remaining subspecies of the grey-crowned rosy-finch are intermixed in the phylogeny, rendering this taxon paraphyletic (check this blog post for an explanation of paraphyly). A taxonomic revision might thus be necessary.

In line with the study by Sergei Drovetski et al. (2009), the researchers also found signatures of gene flow between different populations. This finding can explain why analyses based on a few genes were unable to discriminate between the North American species. The use of genomic data often results to the detection of minor differences between populations, which leads to an important warning. Just because you can discriminate between certain populations with genomic data does not mean they should automatically be considered separate species. Indeed, in a PNAS paper Jeet Sukumaran and Lacey Knowles nicely described this issue: “Until new methods are developed that can discriminate between structure due to population-level processes and that due to species boundaries, genomic-based results should only be considered a hypothesis that requires validation of delimited species with multiple data types, such as phenotypic and ecological information.” The taxonomic story of the American rosy-finches is just getting started.

The distribution (figure a) and phylogenetic relationships between the different rosy-finch taxa (figure d). From: Funk et al. (2020) Systematic Biology.


Funk, E. R., Spellman, G. M., Winker, K., Withrow, J. J., Ruegg, K. C., Zavaleta, E., & Taylor, S. A. (2021). Phylogenomic data reveal widespread introgression across the range of an alpine and arctic specialist. Systematic Biology70(3), 527-541.

Featured image: Gray-crowned Rosy-Finch (Leucosticte tephrocotis) © Alan D. Wilson | Wikimedia Commons

This paper has been added to the Fringillidae page.

A new subspecies of Manx Shearwater from the Canary Islands

But how convincing is the supporting evidence?

A quick question: How many subspecies of Manx shearwater (Puffinus puffinus) are there? If you check the Birds of the World website, you will see the label “monotypic” which means no subspecies have been described. However, this classification might change in the near future. A recent paper in the Journal of Avian Biology presents evidence for a subspecies on the Canary Islands.

Our results show that the Canary Islands population is phenotypically distinguishable from other populations in breeding phenology, biometrics, plumage colouration and acoustics traits. In addition, we found an incipient genetic differentiation, representing a new case of cryptic differentiation of peripheral populations in Procellariiformes.

The core breeding populations of Manx shearwater are located in the United Kingdom and Ireland, with several peripheral populations on islands, such as Iceland, Newfoundland and the Azores. Detailed studies on these island populations might lead to the description of more subspecies. But let’s focus on the new subspecies (Puffinus puffinus canariensis) from the Canary Islands and check the supporting evidence.

Reproductive Isolation?

The researchers compared birds from three locations: Mallaig (Scotland), Corvo (Azores) and La Palma/Tenerife (Canary Islands). First, they looked at fledging date: the Canarian birds fledged on average 31 days earlier than Azorean birds and 52 days earlier than the Mallaig birds. This difference in fledgling date is a common phenomenon in seabirds and is often regarded as a mechanism for (sympatric) speciation. Reproductive isolation can build up when different populations breed at different times (i.e. allochrony). Similar patterns have been reported in other seabird species, such as the storm-petrels (genus Hydrobates, see this blog post).

Another feature that hints at some level of reproductive isolation between different populations of Manx shearwater concerns the sounds that they produce. Acoustic analyses revealed that nine out of twelve acoustic variables were significantly different between the northern population and the Canary Islands. Whether these calls are different enough for the shearwaters to consider birds from other populations as members of a different species remains to be investigated.

Shearwaters from the Canary Islands (blue) fledged earlier compared to birds from the Azores (green) and Scotland (red). From: Rodriguez et al. (2020) Journal of Avian Biology.

Morphology and Genetics

From a morphological point of view, the researchers also documented significant differences. In general, the Canarian birds were lighter and has shorter wings than birds from other populations. In addition, shearwaters from the Canary Islands has darker underwing plumage. Interestingly, these patterns are in line with the Bergmann’s Rule and Gloger’s rule. Bergmann’s Rule states that populations of larger size are found in colder environments, while populations of smaller size occur in warmer regions (see for example this blog post on the line-cheeked spinetail). And Gloger’s Rule describes that more heavily pigmented populations tend to be found in more humid environments, such as near the equator (check out this blog post for more on Gloger’s Rule in gulls).

Finally, genetic analyses of the mitochondrial control region indicated some genetic differentiation between the Canary Islands and the other populations. Eight out of twelve Canarian birds grouped together in the phylogenetic tree, while the remaining four Canarian individuals were scattered across different branches. There is thus some level of genetic differentiation, but the four outliers need to be explained. They might be the result of introgression when birds from different islands interbred, or the outcome of incomplete lineage sorting at the early stages of speciation. Genetic studies with more markers are needed to sort this out.

Genetic analyses showed that most individuals from the Canary Islands cluster together in the phylogenetic tree. Four samples are scattered across the tree and need further investigation. From: Rodriguez et al. (2020) Journal of Avian Biology.

The Subspecies Concept

Based on these thorough analyses, the researchers thus recommended to consider the Canary Island population as a distinct subspecies. The use of subspecies is quite common in ornithology, although it has led to some heated debate in the scientific literature. The application of subspecies names was introduced by Carl Bruch in 1828 to indicate geographically different forms within a species. In the early twentieth century, the system became commonplace due to the promotion of Elliot Coues in America, and Ernst Hartert and Henry Seebohm in Britain. However, in 1953, two entomologists – Edward Osborn Wilson and William Louis Brown Jr. – heavily criticized the subspecies concept, writing that “the subspecies concept is the most critical and disorderly area of modern systematic theory”. The debate continued and is still raging today (see for example, this recent edition of Ornithological Monographs, dedicated to the subspecies concept).

I won’t go into this tricky discussion, but I will highlight one important argument in favor of describing subspecies. Giving certain populations a formal name draws the attention of government officials and can lead to faster action in conservation efforts. Indeed, the authors indicate that “the taxonomic identification of the Canarian Manx shearwater as a new subspecies should lead to prioritisation of its conservation through an action plan.” And by implementing certain measures, such as excluding introduced predators or managing powerlines, we will not only protect the Manx shearwater, but also countless other species on the Canary Islands.


Rodríguez, et al. (2020) Cryptic differentiation in the Manx shearwater hinders the identification of a new endemic subspecies. Journal of Avian Biology51(11).

Featured image: Manx shearwater (Puffinus puffinus) © Martin Reith | Wikimedia Commons

Testing the gradient speciation hypothesis in New Guinea Kingfishers

And how common is this speciation model in birds?

Hybrid zones have often been described as “natural laboratories” that scientists can use to study the origin of new species. Indeed, the formation of a hybrid zone is tightly linked with two geographical modes of speciation: allopatric speciation and parapatric speciation. I briefly discussed these concepts in my PhD thesis:

In allopatric speciation, the geographic range of a species is split in two or more isolated populations that diverge by natural selection or genetic drift. When allopatry is interrupted and the diverging populations have not reached complete reproductive isolation, a secondary hybrid zone can arise. Parapatric speciation concerns the evolution of reproductive isolation between populations that still exchange genes to a limited extent. This mode of speciation comes in two forms: speciation by distance and clinal speciation. In the former, gene flow is reduced as a result of isolation by distance (Mayr, 1942). Over time, the most distant populations differentiate despite a chain of interconnected populations that continue to exchange genes. A special case of speciation by distance concerns ring species, in which the chain of populations is found around a geographical barrier and the populations at the end meet without interbreeding (Irwin et al., 2001). In clinal speciation, a single population can separate into two in response to gradual spatial variation in ecological conditions (Endler, 1977). Both speciation by distance and clinal speciation can lead to the formation of a primary hybrid zone.

The model of clinal speciation can also be applied to elevational series where closely related species have overlapping distributions along an elevational gradient. According to the gradient speciation hypothesis, these elevational series are the outcome of local adaptation to different elevational niches, resulting in the the evolution of reproductive isolation between the parapatric populations. In a recent study in the Journal of Evolutionary Biology, Ethan Linck and his colleagues tested the gradient speciation hypothesis for two kingfisher species in New Guinea: the yellow-billed kingfisher (Syma torotoro) and the mountain kingfisher (S. megarhyncha).


The yellow-billed kingfisher is a lowland forest species that occurs primarily below 700 m, whereas the slightly larger mountain kingfisher can be found above 1100–2200 m or higher in mid-montane forest. The researchers suspected that these species might adhere to the gradient speciation hypothesis for several reasons. First, both species are territorial and sedentary, which might ensure that they don’t disperse far and are thus subject to strong local selection across the steep environmental gradient. Second, the larger size of the mountain kingfisher is consistent with predictions of morphological adaptation to a cooler climate, suggesting local adaptation. And third, some geographically isolated populations of the mountain kingfisher show differences in bill markings, which may be the outcome of parallel evolution along the elevational gradient. If so, we would expect to see several population pairs of yellow-billed and mountain kingfisher that independently adapted to the environmental conditions.

Despite these reasonable arguments, the researchers found no evidence for the gradient speciation hypothesis. Both species form distinct genetic groups with clear acoustic and morphological differences (see figures below). These results contradict the idea that geographically isolated populations of the mountain kingfisher independently adapted to life at higher altitudes. Moreover, the best demographic model indicated a scenario of allopatric speciation with secondary contact.

These analyses reveal that the yellow-billed kingfisher and the mountain kingfisher are distinct species that follow a scenario of allopatric speciation with secondary contact. From: Linck et al. (2020) Journal of Evolutionary Biology.

Literature Search

In addition to unraveling the evolutionary history of these kingfishers, the researchers performed a literature to quantify the generality of the gradient speciation hypothesis in birds. They report that “of the 24 taxa included in our review, 17 concluded secondary contact was the exclusive mechanism behind the formational of elevational replacements. […] All putative cases of gradient speciation lacked corroborating population genomic evidence.” These findings indicate that parapatric speciation along elevational gradients is probably a rare phenomenon in birds.


Linck, E., Freeman, B. G., & Dumbacher, J. P. (2020). Speciation and gene flow across an elevational gradient in New Guinea kingfishers. Journal of Evolutionary Biology33(11), 1643-1652.

Featured image: Yellow-billed kingfisher (Syma torotoro) © markaharper1 | Wikimedia Commons

This paper has been added to the Coraciiformes page.

Rapid morphological evolution in the Silvereye: random processes or selection?

A clever combination of morphological and genomic analyses provide the answer.

Evolution is often depicted as a slow and gradual process that we cannot observe during our lifetime. However, evolutionary changes can happen relatively fast. When a few individuals colonize a new area, they get exposed to novel selective pressures and the population might show rapid morphological changes. In addition, the random sampling effect during the founding event can also speed up evolution. The newly arrived members might be a biased sample from the source population. For example, bigger birds might be more likely to reach an isolated island. It is, however, often extremely difficult to determine whether natural selection or random processes are driving the rapid morphological changes.

One approach is to study a recent colonization event and calculate the Ne* statistic, which was introduced by Lande (1976). This statistic can be applied to a morphological trait and indicates the effective population size that is required to explain morphological shifts by random processes alone. Next, the resulting Ne* can be compared with the actual effective population size (Ne). If this actual population size is larger than the Ne*, then drift is insufficient to explain the morphological changes and selection needs to be invoked.

French Polynesia

Calculating a statistic is relatively straightforward, but where can we find a recent colonization event? In 1937, the aviculturist Eastham Guild introduced the silvereye (Zosterops lateralis) to the island of Tahiti in French Polynesia. The introduced population persisted in low numbers until the late 1950s after which they expanded into all habitat types on the island, and later even dispersed to ten other islands in the archipelago. A recent study in the journal Heredity took advantage of this situation and closely studied morphological evolution of these silvereye populations.

Ashley Sendell-Price and his colleagues measured several morphological traits for almost 200 silvereyes. For each trait, they calculated Lande’s statistic Ne* and compared it with the actual effective population size. These analyses showed that most rapid morphological shifts could be explained by random processes alone. There were, however, some exceptions, such as the morphology of the bill. These exceptions were supported by additional genomic analyses.

Colonisation history of the silvereye across islands of French Polynesia. From Sendell-Price et al. (2020) Heredity.

Candidate Genes

Apart from the morphological analyses, the researchers performed a genomic scan to detect genes under positive selection. This exercise led to a list of 12 candidate genes. Here are the most relevant ones that have been found in other bird species:

  • VPS50: associated with bill length in Berthelot’s pipit (Anthus berthelotii)
  • VPS13B: under directional selection between species of Darwin’s finches
  • NFIA: associated with bill length in the house sparrow (Passer domesticus)
  • PTDSSI: under directional selection in birds of paradise
  • OSR2: experimentally demonstrated to play a role in beak development in birds

The remaining candidate genes (E2F4, FREM2, PBX3, RALGPS1, TMC6 and ZMYND11) are all associated with craniofacial disorders in several non-avian species. Taken together, the morphological and genomic results indicate that the observed morphological shifts within the French Polynesian population of silvereyes are due to a combination of random and selective processes.

Overview of candidate genes under positive selection in different silvereye populations across French Polynesia. From Sendell-Price et al. (2020) Heredity.


Sendell-Price, A. T., Ruegg, K. C., & Clegg, S. M. (2020). Rapid morphological divergence following a human-mediated introduction: The role of drift and directional selection. Heredity124(4), 535-549.

Featured image: Silvereye (Zosterops lateralis) © Bernard Spragg | Wikimedia Commons

Unraveling the genetic basis of adaptive traits in the endangered Hihi

Are these traits encoded by a few genes or many?

“Adapt, move or die.” That is a topic we discuss in the course Climate Change Ecology which I teach with several colleagues at Wageningen University. When the environment changes, some populations can quickly adapt to the new circumstances. The speed and success of adaptation is partly influenced by the genetic basis of the relevant traits. For example, theoretical work suggests that traits encoded by multiple genes can constrain rapid adaptation. With multiple genomic loci, chances are higher that some variation will be lost due to random processes, such as genetic drift. Moreover, some of these potentially adaptive loci might be linked with deleterious alleles, preventing these loci from increasing in frequency. It is thus important to understand the genetic basis of traits in order to predict their response to selection.

A recent study in the Proceedings of the Royal Society B took a closer look at the hihi (Notiomystis cincta), a small songbird endemic to New Zealand. The small population size of this endangered species makes it vulnerable to the effects of genetic drift. Previous work reported three traits are under selection: tarsus length, body mass and head–bill length. How quickly and efficiently these traits can adapt depends on their genetic basis. Are they encoded by a few genes or many?


One way to determine the number of genes underlying is particular trait is to calculate how heritability is distributed across the genome. Heritability refers to the proportion of morphological variation that is explained by genetics. In other words, how much do offspring resemble their parents due to shared genetic variants. This is mostly tested using extensive pedigrees where you can directly compare the morphology of parents and their offspring. In this study, however, the researchers used a genomic relatedness matrix to calculate heritability (you can check out this paper for more details on this method).

Once you have calculated the heritability of a trait, you can check how much each chromosome contributes to this trait. If multiple chromosomes contribute to the genetic variation of a trait, it is likely influenced by multiple genes. In addition, if large chromosomes (which contain more genes) explain a more genetic variation than smaller chromosomes, the trait is probably polygenic.

In the hihi, analyses of the three traits revealed low heritability. It turned out that genetics explains only 13%, 6% and 12% of the morphological variation in tarsus length, body mass and head–bill length, respectively. Moreover, this variation was distributed across several chromosomes, indicating that multiple genes are involved. For two traits (tarsus length and body mass), there was a positive relationship between genetic variation and chromosome size, supporting the conclusion that these traits are influence by multiple genes.

The variation explained by genetic for the three traits is distributed across multiple chromosomes. For two traits (tarsus length and body mass), there is a positive – though not significant – relationship with chromosome size. From: Duntsch et al. (2020) Proceedings B.

Adaptive Potential

A second approach to determine the genetic basis of a trait is a genome-wide association scan (GWAS). This analysis checks which genomic loci are significantly associated with particular traits. If a trait with significant heritability has no significant GWAS peaks, the trait is probably polygenic. The researchers found no genetic variants that were significantly associated with any of the three traits, following the conclusions of the other analyses that these traits are influenced by multiple genes. For each trait, however, there were several genetic variants of interest (despite not being significant). For example, the genetic variant most strongly associated with tarsus length can be found in an intronic region of the HEY2 transcription factor which is involved in embryological development.

The information about the genetic basis of the three traits can help researchers to predict the rate of adaptation of this endangered species, and take appropriate conservation measures. The authors conclude:

We have demonstrated that many loci of small effect are likely to contribute the majority of variation to all three morphological traits. Given the small effective population size of all hihi populations, many adaptive variants are likely to be lost to drift at a rate that is faster than the input of new variation via mutation. This is likely to slow the speed of adaptation and lead to further constraint on the adaptive potential of the species.


Duntsch, L., Tomotani, B. M., de Villemereuil, P., Brekke, P., Lee, K. D., Ewen, J. G., & Santure, A. W. (2020). Polygenic basis for adaptive morphological variation in a threatened Aotearoa| New Zealand bird, the hihi (Notiomystis cincta). Proceedings of the Royal Society B287(1933), 20200948.

Featured image: Hihi (Notiomystis cincta) © Judi Lapsley Miller | Wikimedia Commons

Bad news for the Brown Eared Pheasant?

Genomic study finds low genetic diversity and high levels of inbreeding in this vulnerable species.

Small populations are often at risk. They can get sucked in a negative feedback loop of genetic and demographic decline that culminates in their extinction (the so-called extinction vortex, which I covered in this blog post). In general, small populations are more vulnerable to genetic drift and inbreeding, leading to a loss of genetic diversity. This lower level of genetic diversity might prevent small populations from adapting to changing environments. However, it is not all misery and mayhem for small populations. One potential benefit of a small population size is genetic purging, the process in which deleterious variants appear more often due to inbreeding and get purged from the population because individuals carrying these variants fail to survive or reproduce. The result is a genetically healthier population, despite low levels of genetic diversity.

A recent study in the journal Molecular Biology and Evolution examined the situation of the brown eared pheasant (Crossoptilon mantchuricum), a vulnerable bird species that is declining across its range in China due to human activities, such as deforestation and hunting. Is this species heading for extinction or does it reap the benefits of genetic purging?

Genetic Purging?

Based on the genomes of 40 individuals, the researchers identified three distinct populations corresponding to locations in Shaanxi (Western), Shanxi (Central), and Hebei & Beijing (Eastern). The genetic diversity across these three populations was extremely low. In fact, it was the lowest genome-wide estimate for any bird species to date. But, as explained above, this low level of genetic diversity might result in genetic purging when deleterious alleles are filtered out by purifying selection.

The action of genetic purging can be tested with the population genetic statistic Tajima’s D. I have explained the rationale behind the statistic in another blog post, but for this story you only need to understand the main interpretation. In general, a negative Tajima’s D points to a selective sweep (and thus genetic purging), while a positive Tajima’s D suggests balancing selection. In the three brown eared pheasant populations, Tajima’s D was highly positive. There is thus no evidence for genetic purging. And that is bad news…

The brown eared pheasant shows very low levels of genetic diversity (left figure). The positive values of Tajima’s D suggest that there is little purifying selection across the genome of this species (right figure). Blue refers to the blue eared pheasant, Brown-W, Brown-C and Brown-E refer to three populations of the brown eared pheasant. Adapted from Wang et al. (2021) Molecular Biology and Evolution.

Genetic Load

Low genetic diversity is often the outcome of inbreeding. When related individuals mate, their offspring will mostly receive the same genetic variants from both parents. This results in large genomic regions with little genetic variation, also known as runs of homozygosity (ROHs). The brown eared pheasant did indeed show more ROHs compared to its sister species, the blue eared pheasant (C. auritum), that is of little conservation concern.

A closer look at these genomic regions revealed that some brown eared pheasant populations have accumulated missense and loss-of-function mutations. Missense mutations occur when a change in the DNA results in the wrong amino acid being incorporated into a protein. And loss-of-function mutations lead to functional problems in the activity of a protein. Clearly, the brown eared pheasant is suffering from inbreeding depression. Moreover, because natural selection seems unable to eliminate deleterious mutations, this species is accumulating a high genetic load. Unless conservation actions are implemented – such as a genetic rescue program – the brown eared pheasant might be heading for extinction.

The brown eared pheasant populations show more runs of homozygosity (ROHs) compared to the blue eared pheasant, suggesting high levels of inbreeding. From: Wang et al. (2021) Molecular Biology and Evolution.


Wang et al. (2021). Genomic Consequences of Long-Term Population Decline in Brown Eared Pheasant. Molecular Biology and Evolution38(1), 263-273.

Featured image: Brown eared pheasant (Crossoptilon mantchuricum) © Josh More | Flickr