A front-row seat to evolution: What common barn swallows can teach us about how new species form | CU Boulder Today | University of Colorado Boulder
This paper in Science passed me by last December but it's too good to ignore because it is an example of something that creationists insist has never been seen because it doesn't happen - evolution in progress. And, to annoy creationists even more, it's an example of something Charles Darwin proposed as a mechanism for speciation - mate selection - as the isolating mechanism.
Barn swallows are one of the species that has formed a commensal relationship with humans that does not, like many other commensal species, involve it in consuming our crops either in the fields or in storage, from when we began building permanent or semi-permanent buildings. They are now dependent on our barns and out-houses as nesting places.
What can you tell me about the subspecies of barn swallow, Hirundo rustica, their commensal relationship with humans and their evolution into different subspecies? The barn swallow (Hirundo rustica) is a widely distributed passerine bird with several recognized subspecies that have evolved in different geographic regions. Their evolution and divergence into subspecies have been shaped by geographical isolation, ecological adaptation, and their long-standing commensal relationship with humans.News of how they are in the process of speciating comes in the form of a paper in Science by a team led by Professor Rebecca Safran, the paper’s senior author and professor in the Department of Ecology and Evolutionary Biology at the University of Colorado Boulder, and an article in CU Boulder Today by Yvaine Ye:
Subspecies of the Barn Swallow (Hirundo rustica)
There are six generally recognized subspecies, each adapted to different regions:
- H. r. rustica – Nominate subspecies
- Breeds in Europe and Asia (west of the Urals) and winters in Africa and South Asia.
- Characterized by a long, deeply forked tail and a reddish forehead and throat.
- H. r. transitiva
- Found in the Levant (Middle East, particularly Israel and Palestine).
- Slightly darker underparts and a shorter tail compared to H. r. rustica.
- H. r. savignii
- Endemic to Egypt.
- Has shorter tail streamers and a darker, more intense red coloration on the throat and forehead.
- H. r. gutturalis
- Breeds in East Asia (Japan, China, Korea, and parts of Russia) and winters in Southeast Asia.
- Has a paler underbelly and slightly shorter tail than H. r. rustica.
- H. r. tytleri
- Breeds in central Asia (from the Altai Mountains to Mongolia and northeast China) and winters in South Asia.
- Larger body size, darker plumage, and a more pronounced reddish throat.
- H. r. erythrogaster
- Found in North America, migrating to Central and South America in winter.
- Has a deeper red or orange belly and a more robust body compared to Old World subspecies.
Commensal Relationship with Humans
Barn swallows have one of the most well-documented commensal relationships with humans among birds. Unlike many species that avoid human settlements, barn swallows have thrived in human-altered environments, particularly in agricultural landscapes.
How They Benefit from Humans:
Human Benefits:
- Nesting Sites: They originally nested in caves and rocky outcrops but now prefer human-made structures such as barns, bridges, and eaves of houses. This shift has expanded their range and allowed for increased breeding success.
- Foraging Opportunities: Agricultural areas provide open fields where they can hunt flying insects more efficiently.
- Predator Protection: Nesting near human settlements reduces predation by natural enemies such as corvids and raptors.
- Pest Control: Barn swallows consume vast numbers of flying insects, including mosquitoes and agricultural pests, making them beneficial to farmers.
- Aesthetic and Cultural Value: Many cultures associate barn swallows with good luck and the arrival of spring.
Evolution and Subspecies Divergence
The divergence of barn swallow subspecies is a classic example of allopatric speciation (geographical isolation) and ecological adaptation:While the different subspecies show clear distinctions in plumage, size, and migratory behavior, they still interbreed where their ranges overlap, maintaining them as a single species rather than diverging into separate species.
- Glacial and Post-Glacial Expansion:
- During the last Ice Age, populations were likely confined to refugia in warmer regions. As glaciers receded, they expanded into new territories, leading to genetic divergence.
- Geographical Barriers:
- Mountain ranges (e.g., the Himalayas), deserts, and oceans have limited gene flow between populations, leading to the formation of distinct subspecies.
- Adaptation to Local Environments:
- Differences in climate, insect availability, and nesting opportunities have influenced morphological and behavioral traits.
- For example, H. r. erythrogaster in North America has evolved a more vibrant belly color, possibly due to sexual selection pressures differing from those in Europe.
- Human Influence:
- Their close association with human settlements has likely accelerated their spread and may have contributed to gene flow between some subspecies.
Conclusion
The barn swallow is a remarkable example of how a species can adapt to human presence and expand its range globally. Their subspecies have evolved due to historical climatic events, geographical isolation, and ecological pressures, yet they remain a single, highly mobile species with a complex migratory and commensal relationship with humans.
A front-row seat to evolution: What common barn swallows can teach us about how new species form
Beauty is in the eye of the beholder—even if that beholder is a barn swallow.
Depending on where the birds live, some of them may favor mates with a paler chest color while others find a redder chest more attractive. The difference in what these birds prefer when it comes to choosing a mate is helping scientists unlock one of biology’s greatest mysteries: How do new species originate?
In a new CU Boulder-led study, biologists used genetic sequencing from barn swallows around the globe to provide real-time evidence that sexual selection, in which organisms choose mates based on traits they find attractive, drives the emergence of new species.
The study was published Dec 12 in the journal Science.
This is one of the very first papers to comprehensively show the role of mate selection decisions in the evolution of new species.
Professor Rebecca Safran, senior author
Department of Ecology and Evolutionary Biology
Colorado University Boulder
Boulder, Colorado, USA.
The new findings shed light on how new species form, a fundamental but elusive process for all life on Earth.
Proving Darwin right
Charles Darwin proposed the theory of sexual selection in 1875. It suggests that organisms evolve showy traits, like extravagant plumage or eye-catching dance moves, to attract mates. When organisms of the same species develop preferences for different traits and no longer breed with each other, new species could emerge over time, a process known as speciation.
For the past 150 years, researchers of sexual selection have primarily studied organisms that already diverged into distinct species. For example, orchids, which now encompass more than 25,000 species, originated from a common ancestor. Their remarkable diversity often leads to the assumption that they evolved different looks to attract different pollinators, said Drew Schield, the paper’s first author and assistant professor at the University of Virginia.
It’s logical to think this way and it could totally be the case, but with speciation already having occurred, it’s impossible to know for certain.
Assistant Professor Drew Schield, first author
Department of Ecology and Evolutionary Biology
University of Colorado, Boulder, CO, USA. Now at the Department of Biology
University of Virginia, Charlottesville, VA, USA.
As a result, it has been difficult to find direct evidence that sexual selection drives the emergence of new species.
Barn swallows provide a unique opportunity to explore the speciation process as it unfolds.
These birds are one of the most common and widespread species on our planet. Currently, there are six subspecies of barn swallow each looking slightly different in some traits critical to the mate choice decisions depending on where they are.
For example, the East Asian group, Hirundo rustica gutturalis, has a pale chest and shorter tail streamers—the elongated outer tail feathers. Hirundo rustica tytleri, found in Siberia, has long tail streamers and red chest feathers. The subspecies in Europe and western Asia, Hirundo rustica rustica, has a pale chest and long tail streamers.
Reuniting after isolation
Evidence suggests that the bird’s ancestors left the Nile River valley in northern Africa about 11,000 years ago and spread out across the Northern Hemisphere. For thousands of years, different populations barely interacted and developed diverse traits, forming subspecies.
Some 800 to 2000 years ago, certain subspecies expanded their territories, and habitats began to overlap. In some parts of the world, subspecies now interact with each other, producing hybrid offspring.
Safran and her team set out to investigate whether sexual selection in these birds was driving the speciation process.
The team, including Elizabeth Scordato, associate professor at the California State Polytechnic University, sequenced the genomes of 336 barn swallows from around the globe, encompassing all subspecies and three hybrid zones, where subspecies interbreed, in Eurasia.
The researchers found a dozen regions in the barn swallow genome associated with the birds’ two sexually selected traits: Ventral coloration—the plumage color of their chest and belly— and tail streamer length.
When individuals reproduce, the genes from both parents reshuffle and combine to form the genes of their offspring. When two populations encounter one another, the flow of genetic material from one to another is a marker of how similar the populations are. If the rate of gene flow is low, it means the two populations are breeding with each other at a lower rate than they would if they are the same species.
The study found that in barn swallow hybrid zones much of their genes flows freely across groups. But the genetic regions coding for ventral coloration and tail streamer length hardly transfer to other populations.
It suggests that among the hybrid individuals with parents from different subspecies, a small number of lucky birds that inherit a favorable combination of tail streamer and ventral color genes are able to attract mates. Hybrids that receive less favorable combinations tend to be less successful in reproduction.
The different preferences for tail feather length and chest color across subspecies make barn swallows more likely to mate within their own group, Schield added. If the trend continues, these groups could no longer interbreed or produce offspring, markers for the formation of separate species.These genes are hitting a boundary due to divergent sexual selection, and they stop moving from one population to the other.
Assistant Professor Drew Schield.
Next, the team plans to sample more birds and study whether being a hybrid affects reproductive success.
It’s very cool that we could capture a real-time evolutionary portrait of this common animal and understand how and why the populations are diverging. Our understanding of the process is fundamentally important for addressing a wide range of questions related to biodiversity, evolution and conservation.
Professor Rebecca Safran.
So, there we are; as good an example as any creationist would wish to ignore, of observed evolution in progress as the barn swallow diversifies into species which then become species as barriers to geneflow evolve to ensure complete genetic isolation. And an example of how, as the process of speciation progresses, interbreeding is still possible when the process is sympatric, in other words, where the two gene pools are not physically isolated. This is pretty much how human speciation occurred both in Africa and in Eurasia when Homo erectus followed by H. sapiens migrated there.Structured Abstract
INTRODUCTION
Assessing how sexual traits and their genetic basis contribute barriers to gene flow in secondary contact due to effects on hybrid fitness remains critical to establishing a causal role of sexual selection in in speciation. Leveraging natural systems with intraspecific variation in sexual traits at early stages of the speciation process holds promise for identifying links between patterns of phenotypic and genomic variation and the evolution of reproductive isolation.
RATIONALE
Observational and experimental studies indicate that barn swallows (Hirundo rustica) are a robust empirical model of divergent sexual selection and that the presence of multiple hybrid zones between populations in Eurasia enables investigation of barriers to gene flow. We investigate genotypic and phenotypic variation in barn swallows to (i) map the genetic basis of plumage traits used in sexual signaling, (ii) test whether loci underlying sexual traits have experienced divergent sexual selection in allopatry and present barriers to gene flow in secondary contact, and (iii) test the prediction that sexual selection has maintained linkage disequilibrium (LD) between barrier loci in secondary contact as a result of their effects on hybrid fitness.
RESULTS
We sequenced the genomes of 336 barn swallows sampled across the breeding distribution of the species and quantified variation in ventral coloration and tail streamer length, two signal traits used in mate choice. Populations differ in these traits and hybrids between the subspecies rustica, tytleri, and gutturalis exhibit phenotypes that are intermediate between or similar to parental populations. The genetic architecture of ventral color is concentrated on chromosome 1A and the Z chromosome whereas phenotypic variation is largely explained by genotypic variation at 10 loci, including the melanogenesis genes KITLG, SLC45A2, and BNC2. Variation in tail streamer length is explained by loci on chromosome 2. Sexual trait loci—ventral color loci in particular—exhibit peaks of high differentiation between populations and signatures of divergent positive selection in allopatry. We further investigated whether loci under divergent sexual selection contribute barriers to gene flow in secondary contact using geographic and genomic cline analyses across hybrid zone transects, finding that sexual trait loci constitute barriers in the rustica-tytleri and rustica-gutturalis hybrid zones whereas gene flow is less constrained across the remainder of the genome. Clines for sexual trait loci in these hybrid zones also show a high degree of concordance, consistent with selection for specific combinations of alleles from parental populations in hybrids. Finally, we tested whether selection has generated ongoing coupling of barrier loci by investigating LD patterns in hybrid zones. These tests reveal elevated LD among sexual trait barrier loci in hybrids beyond what is expected under admixture alone, consistent with the genetic coupling of barriers being an emergent property of divergent sexual selection.
CONCLUSION
Our findings demonstrate an important role for sexual selection in speciation through the analysis of the genomic basis of sexual signal traits in barn swallows, evidence for divergent selection in geographic isolation, and evidence that loci underlying traits involved in prezygotic isolation represent barriers to gene flow. Our results further support the conclusion that the genetic coupling of sexual trait loci generated by selection promotes reproductive isolation upon secondary contact.
Abstract
Despite the well-known effects of sexual selection on phenotypes, links between this evolutionary process and reproductive isolation, genomic divergence, and speciation have been difficult to establish. We unravel the genetic basis of sexually selected plumage traits to investigate their effects on reproductive isolation in barn swallows. The genetic architecture of sexual traits is characterized by 12 loci on two autosomes and the Z chromosome. Sexual trait loci exhibit signatures of divergent selection in geographic isolation and barriers to gene flow in secondary contact. Linkage disequilibrium between these genes has been maintained by selection in hybrid zones beyond what would be expected under admixture alone. Our findings reveal that selection on coupled sexual trait loci promotes reproductive isolation, providing key empirical evidence for the role of sexual selection in speciation.
Schield, Drew R.; Carter, Javan K.; Scordato, Elizabeth S. C.; Levin, Iris I.; Wilkins, Matthew R.; Mueller, Sarah A.; Gompert, Zachariah; Nosil, Patrik; Wolf, Jochen B. W.; Safran, Rebecca J. (2024)
Sexual selection promotes reproductive isolation in barn swallows
Science; 386(6727) eadj8766; DOI: 10.1126/science.adj8766
Copyright: © 2024 The authors.
Published by American Association for the Advancement of Science. Open access.
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)