Studying the global conquest of the Common Starling with haplotype networks

Recent study compares the genetic diversity of three independent invasions.

If there is one species that deserves the adjective “common” in its name, it is definitely the Common Starling (Sturnus vulgaris). This noisy songbird can be found on every continent (except Antarctica). Starlings are native to the Palearctic but have been repeatedly introduced in other locations. In a previous blog post, I described how the Common Starling conquered Australia where it spread across the island after its release in the 1850s. Similar introductions occurred in North America as part of an American Acclimatization Society initiative to populate Central Park with the birds from Shakespeare’s plays. This initiative led to the release of 60 individuals in 1890 and an additional 40 in 1891. The introduction in South Africa was more modest with about 18 individuals being released around 1897. In each case, the starlings managed to get a foothold and establish stable populations. Their success has been attributed to their generalist diet and their ability to quickly change their migratory behavior.

These three independent introduction events (North America, Australia and South Africa) all started with small populations that quickly expanded. How has this impacted the genetic make-up of the current starling populations? A recent study in the journal Ecology and Evolution compared genetic diversity at the mitochondrial control region to answer this question.

Haplotypes

Before we dive into the results of this study, we need to understand the concept of a haplotype. This commonly used term refers to a DNA sequence of genetic variants that are inherited as a whole. By comparing different haplotypes and identifying particular mutations, we can construct a haplotype network that visualizes the connections between the haplotypes. Imagine that we sequenced a short DNA sequence in four individuals:

  • Individual 1: AAAA
  • Individual 2: AAAA
  • Individual 3: AATA
  • Individual 4: AATC

We can clearly see that individuals 1 and 2 have the same haplotype (AAAA) while individual 3 has one mutation (T instead of A) and individual 4 has two mutations (TC instead of AA). The relationships between these four individuals can be depicted by circles (representing the haplotypes) connected by lines. The size of the circles indicates the number of individuals with a particular haplotype and the length of the line signifies the number of mutations separating two haplotypes. Hence, the haplotype network for our example looks like this. The different colors indicate the sampling locations: individuals 1, 2 and 3 come from one area (in blue), whereas individual 4 was found somewhere else (in green).

An example of a haplotype network. See text for the explanation.

Source Populations

The researchers constructed a haplotype network using almost 1000 samples from North America, Australia, South Africa and the United Kingdom. They found a total of 64 unique haplotypes that revealed some interesting patterns. In the haplotype network, the South African samples form a separate cluster (in light gray) from the other locations. A more detailed look at the network shows that only one haplotype (H25) is shared by the other two non-native areas, namely North America and Australia. These results suggest that the different introduction events used Common Starlings from different parts of the United Kingdom. To pinpoint the exact source populations, more genetic data is needed.

A network of Common Starlings from the native-range (United Kingdom, black) and three invasive populations (North America, dark gray; Australia, white; South Africa, light gray) constructed using 928 bp of mitochondrial control region haplotypes. From: Bodt et al. (2020) Ecology and Evolution.

Population Expansion

Unsurprisingly, all three invasive populations showed a reduction in genetic diversity compared to the native populations from the UK, reflecting the genetic bottlenecks that occurred at the onset of the introductions. This finding indicates that a low level of genetic diversity of no insurmountable obstacle for the rapid spread of the Common Starling. However, not all invasive populations showed genetic signatures of this expansion. The researchers found genetic support for population expansion in both North America and Australia, but the analysis of South African data did not support a sudden expansion model. Possibly, the South African population is still in a lag-phase following the introduction. The population might be slowly expanding until it reaches a certain threshold that triggers a more explosive expansion. Or the spread of South African starlings is being slowed down by other processes, such as adverse climatic conditions or competition with native species. As always, more research is needed to figure this out. And while ornithologists keep studying these invasions, the Common Starlings will probably keep expanding.

The worldwide distribution of the Common Starling. From: Wikimedia Commons.

References

Bodt, L. H., Rollins, L. A., & Zichello, J. M. (2020). Contrasting mitochondrial diversity of European starlings (Sturnus vulgaris) across three invasive continental distributions. Ecology and Evolution10(18), 10186-10195.

Featured image: Common Starling (Sturnus vulgaris) © Pierre Selim | Wikimedia Commons

The importance of taxonomy in saving the critically endangered Black-winged Myna

The taxonomic decision has important consequences for breeding programs.

The black-winged myna (Acridotheres melanopterus) is almost extinct in the wild. This species contains three subspecies: one subspecies (melanopterus) is practically extinct in the wild except for a small flock inside a Javan wildlife park, while the other two subspecies (tricolor and tertius) each number less than 200 individuals in the wild. Captive breeding programs have been established the safeguard the future of the black-winged myna. However, a recent taxonomic decision by the IUCN has complicated the conservation efforts of these breeding programs. Based on differences in plumage patterns and biometrics, the IUCN decided to elevate the three subspecies to species level. A decision that is not unanimously supported within the IUCN’s Asian Songbird Trade Specialist Group.

This taxonomic change has important implications for captive breeding strategies. The recognition of three species leads to a three small populations for breeding, increasing the risk of genetic inbreeding. Considering three subspecies opens the opportunity to a bigger breeding population (with the possibility of crossing subspecies), but might result in the loss of evolutionarily unique lineages due to hybridization. A recent study in the journal Scientific Reports tried to solve this dilemma with a genomic perspective on the black-winged myna complex.

Genomic Gradient

Keren Sadanandan and her colleagues sequenced thousands of genome-wide markers from 85 captive individuals across the morphological spectrum of the black-winged myna. The genetic analyses pointed to two population clusters: one cluster with melanopterus individuals from western Java and morphological hybrids (between melanopterus and tricolor), and a second containing tertius individuals from Bali. Moreover, the melanopterus individuals and hybrids were distributed along a gradient with varying levels of shared ancestry with the tertius cluster. These results thus show a smooth genomic cline from melanopterus in western Java to tertius in Bali. This clinal pattern does not support the IUCN’s decision to recognize three species (check out this paper for more on the dangers of clinal variation in taxonomy). The classification into three subspecies is further supported by low differentiation of the mitochondrial gene ND2 (less than 1.5%) which does not exceed the mitochondrial divergence threshold typically used for the species level (2-3%).

Genomic analyses uncovered a genomic cline from melanopterus to tertius individuals. From: Sadanandan et al. (2020) Scientific Reports.

Melanistic Introgression?

Additional analyses suggested ancient introgression between the Javan Myna (A. javanicus) and the tertius subspecies on Bali. It is possible that the genomic regions underlying black plumage introgressed from the dark Javan Myna into the most melanistic tertius subspecies. The researchers could not pinpoint the exact introgressed regions, so this hypothesis remains to be tested. Nonetheless, the findings of this study indicate that melanism (the degree of black plumage) does not reflect the genomic differentiation between the three subspecies and is thus not a reliable character for taxonomic decisions. This leads the researchers to the following conclusion:

Our study showed that the two geographically and morphologically terminal forms of BWM, melanopterus in the west and darker tertius in the east, are characterized by a mtDNA divergence below the species level. Variation in levels of melanism, recently used to separate BWMs into three species, is not reflected by deep genomic differentiation, arguing in favour of the traditional taxonomic arrangement that unites all three forms as subspecies rather than species.

What does this mean for the breeding programs? The researchers recommend “three separate breeding sub-programs under the umbrella of a single species-wide program without a strict separation.” This will hopefully preserve the range of morphological and genetic diversity within the black-winged myna.

References

Sadanandan, K. R., Low, G. W., Sridharan, S., Gwee, C. Y., Ng, E. Y., Yuda, P., Prawiradilaga, D. M., Lee, J. G. H., Tritto, A. & Rheindt, F. E. (2020). The conservation value of admixed phenotypes in a critically endangered species complex. Scientific reports10(1), 1-16.

Featured image: Black-winged Myna (Acridotheres melanopterus) © Doug Jasonjj | Wikimedia Commons

This paper has been added to the Sturnidae page.

How the Common Starling conquered Australia

Genetic population structure is mainly shaped by distance effects.

European settlers introduced several animals to Australia for transportation or farming purposes, while others were brought in as pets or for hunting. From the 1850s onward, Common Starlings (Sturnus vulgaris) were released in several locations, such as Melbourne, Brisbane and Adelaide. Although they lost their ability to migrate, these birds managed to get a foothold and spread across the island. The population dynamics during this invasion shaped the current genetic make-up of Common Starlings in Australia.

It is possible that the introduced populations already differed genetically and diverged even more during the invasion. This divergence can follow a neutral path of isolation-by-distance where neighboring populations continue to exchange gene while distant ones accumulate genetic differences. Or perhaps different populations adapted to local conditions in distinct environments, resulting in isolation-by-environment. A recent study in the journal Molecular Ecology tested these patterns using 568 starling samples from 24 localities across Australia.

Two Clusters

The genetic analyses uncovered two main clusters that correspond to southern Australia (from Western Australia to Tasmania) and northern Australia (New South Wales and southern Queensland). These two groups are separated by an extremely arid region between Victoria and New South Wales. Interestingly, the Great Dividing Range – a mountain range in the east – did not have a big effect on the population genetic structure, suggesting that Common Starlings can cross this mountainous area. If you are not familiar with the geography of Australia, you can check out the map below.

A match between introduction site and genetic ancestry indicated that the genetic make-up of the founder populations partly influenced the present-day patterns. However, the main process shaping the genetic population structure of the Common Starling appears to be isolation-by-distance. As these birds spread across Australia, gene flow between distant populations diminished, giving rise to the correlation between genetic and geographical distance we see today.

Figure a given an overview of the introduction sites (blue dots) and sightings of Common Starlings (grey dots) on eBird. Figure b shows the genetic population structure of the Common Starling, revealing two main groups (red and blue outline). The Great Dividing Range is indicated with a dark blue line. From: Stuart et al. (2021) Molecular Ecology.

Candidate Genes

The authors reported that isolation-by-environment was not significantly correlated with genetic differentiation. This finding can be explained by phenotypic plasticity (i.e. one genotype produces more than one phenotype when exposed to different environments) or by local adaptation driven by a small number of genetic loci. The latter explanation is supported by further analyses in which the researchers tested for genetic variants under positive selection. This search uncovered “several hundred unique candidate loci (375) for local adaptation” and “a total of 25 proteins were identified”. These candidate loci were associated with differences in aridity, precipitation and temperature, suggesting that these environmental factors may be important in driving adaptive variation across the Common Starling’s invasive range.

The paper discusses a few of these candidate genes, such as CACNA1C which plays a role in behavioral plasticity (an important trait for an invading species). However, I always remain reluctant to tell “Just So Stories“. The uncovered genes are interesting starting points for further research, but not the final story. Moreover, the authors also write that “many of the loci were reported for only one of the exploratory methods, and all the annotated proteins identified were unique to their identification method.” More analyses are thus needed to understand the detailed genetic consequences of the Common Starling’s conquest across Australia.

Several genetic loci correlated with particular environmental factors, making them interesting candidates for further research. From: Stuart et al. (2021) Molecular Ecology.

References

Stuart, K. C., Cardilini, A. P., Cassey, P., Richardson, M. F., Sherwin, W. B., Rollins, L. A., & Sherman, C. D. (2021). Signatures of selection in a recent invasion reveal adaptive divergence in a highly vagile invasive species. Molecular Ecology30(6), 1419-1434.

Featured image: Common Starling (Sturnus vulgaris) © Marie-Lan Nguyen | Wikimedia Commons