Ancient DNA reveals low levels of past genetic diversity in the Andean Condor

Low genetic diversity might be the natural state for this vulture.

Since the first release of Andean Condors (Vultur gryphus) in Colombia in 1989, more than 200 individual birds have be re-introduced in the wild across South America. The goal of these introductions was to reinforce existing populations and re-establish extinct ones. One of the main arguments for such extensive management programs is the augmentation of genetic diversity. However, the relationship between genetic diversity and the risk of species extinction is not always straightforward (see for example this blog post). And in many cases, it is not clear how much genetic variation has been lost over time. So, what about the Andean Condor? A recent study in the journal Ecology and Evolution obtained DNA samples from museum collections to assess the historical levels of genetic diversity in this iconic vulture species.

Haplotypes

Julian Padró and his colleagues sequenced several mitochondrial markers for 42 Andean Condors, covering a time period from 1884 to 2013. The historical and modern samples shared several haplotypes, but one haplotype from 1896 seems to have been lost. This genetic variant belonged to a now extinct population on the Patagonian coast. Demographic analyses indicated that this loss of genetic diversity coincided with the timing of European colonization in South America. Probably, the development of livestock production resulted in conflict between humans and Andean Condors.

In contrast to the southern populations, Andean Condors in the north of their range did lose any haplotypes, despite being driven to near-extinction in recent times. The similar genetic diversity in historical and present times, in combination with the relatively modest loss of one mitochondrial haplotype, suggest that the Andean Condor can cope with low levels genetic diversity. Similar patterns have been reported in other raptor species, such as the Spanish Imperial Eagle (Aquila adalberti) and the Cinereous Vulture (Aegypius monachus).

An overview of the sampling locations for the historical and contemporary samples. The haplotype shows the modest loss of genetic diversity over time. From: Padró et al. (2020) Ecology and Evolution.

Genomics

The researchers concluded that “Low levels of genetic diversity found in the Andean condor represent a natural state of mtDNA, and thus are unlikely to be an immediate threat to long-term viability.” However, mtDNA represents only a tiny fraction of the total genetic diversity in a population. A genomic perspective is needed to assess the impact of population bottlenecks on the genetic make-up of the Andean Condor. These raptors might be able to withstand a decline in mitochondrial diversity, but what if other genomic regions have been eroded?

References

Padró, J., Lambertucci, S. A., Perrig, P. L., & Pauli, J. N. (2020). Andean and California condors possess dissimilar genetic composition but exhibit similar demographic histories. Ecology and Evolution, 10(23), 13011-13021.

Featured image: Andean Condor (Vultur gryphus) © Ltshears | Wikimedia Commons

The mystery of the white-faced Limestone Wren-babbler: a leucistic morph or a separate (sub)species?

Genomic and acoustic analyses of the species complex provide the first clues.

Somewhere in Myanmar, there is a white-faced population of the Limestone Wren-babbler (Napothera crispifrons). Ornithologists are not sure how to treat this population from a taxonomic point of view. Is it just a white morph or does it represent a distinct (sub)species? In addition to this mystery, the taxonomy of the Limestone Wren-babbler has been recently revised. Traditionally, this inconspicuous passerine was considered as a single species, comprised of three allopatric subspecies (crispifrons, annamensis and calcicola). However, analyses of plumage differences based on museum specimens suggested to split it into two species: the rufous-bellied N. calcicola and the grey-bellied N. crispifrons (containing two subspecies). An integrative approach is needed here, combining different data sources to support a taxonomic decision (see for example this blog post). And indeed, a recent study in the journal Molecular Ecology collected data on vocalizations and genomics to solve this puzzle.

Three Lineages

Chyi Yin Gwee, Qiao Le Lee and their colleagues generated genomic sequences for 15 individuals and uncovered three deeply divergent lineages. They could confidently discriminate between crispifrons from Myanmar and western Thailand, annamensis from Vietnam and calcicola from northeastern Thailand. More detailed analyses indicated that there has been no gene flow between these three lineages, suggesting that they have been reproductively isolated for some time. The genomic results contradict the plumage-based classification which combined the subspecies annamensis and crispifrons. It turns out that annamensis is more closely related to calcicola than to crispifrons. This finding nicely illustrates the dangers of solely relying on morphological data.

The acoustic data supported the genomic patterns. Analyses of 10 vocal parameters showed that annamensis produces sounds similar to calcicola. Because these taxa look quite different – annamensis is grey-bellied, while calcicola is rufous-bellied – vocal differences might be less important in species recognition. Based on these results, the researchers concluded that “the Limestone Wren-babbler complex consists of three mitochondrially and genomically diverged lineages, each supported by a combination of plumage and vocal characters that would allow them to be diagnosed as different species under many species concepts.”

Genomic analyses of the Limestone Wren-babbler species complex indicated three distinct lineages (see K=3 graph in figure a). Acoustic data separated crispifrons fro the other two taxa (figures b and c), which are morphologically distinct. From: Gwee et al. (2021) Molecular Ecology.

The White Mystery

And what about the white-faced population in Myanmar? The genomic data cluster it within the brown-plumaged populations of crispifrons. Comparing the genomes of white and brown individuals pointed to several outlier regions that contain a few candidate genes involved in pigmentation (including RAB3IP and SLC16A3). Research on other bird species has shown that a few genomic loci can drive drastic plumage differences (see for instance crows and warblers). At the moment, it is difficult to judge how stable the white-faced population is. The researchers might have captured the beginning of a diversification process between white and brown Limestone Wren-babblers, or the white-faced population might disappear in a few generations due to stochastic processes. Only time will tell.

References

Gwee, C. Y., Lee, Q. L., Mahood, S. P., Le Manh, H., Tizard, R., Eiamampai, K., Round, P. D. & Rheindt, F. E. (2021). The interplay of colour and bioacoustic traits in the differentiation of a Southeast Asian songbird complex. Molecular Ecology, 30(1), 297-309.

Featured image: Limestone Wren-babbler (Napothera crispifrons) © Francesco Veronesi | Wikimedia Commons

Does disrupted gene expression cause hybrid sterility in Flycatchers?

Taking a closer look at gene expression in the testis.

Every student of speciation should be familiar with the Bateson-Dobzhansky-Muller (BDM) model of genetic incompatibilities. Most evolutionary biologists can probably explain the rationale behind this model, but not everyone will know its interesting history (and why I chose to list these three names). The model was formulated by Dobzhansky (1934) and further developed by Muller (1942). However, Bateson (1909) already published an essentially identical model, apparently unknown to Dobzhansky and Muller, to explain the “secret of interracial sterility”. The BDM-model is very intuitive. Here is the short version from my PhD thesis:

Consider two allopatric populations diverging independently, with the same ancestral genotype AABB in both populations. In one population, a mutation (A -> a) appears and goes to fixation, resulting in aaBB, which is fertile and viable. In the other population, another mutation (B -> b) appears and goes to fixation, resulting in AAbb, which is also fertile and viable. When these populations meet and interbreed, this will result in the genotype AaBb. Alleles a and b have never “met” each other and it is possible that allele a has a deleterious effect that becomes apparent when allele b is present, or vice versa. Over evolutionary time, numerous of these incompatibilities may arise, each possibly contributing to hybrid sterility or unviability.

This model has been mostly applied to mutations in protein-coding genes, but could be extended to the regulation of gene expression. Regulatory regions come in two main types: cis-regulatory elements that are linked to nearby genes and trans-regulatory elements that affect distant genes (millions of DNA-letters apart). Interacting cis- and trans-regulatory elements often evolve in concert, and a mutation in one element can be compensated by a mutation in the other element. When species have experienced different compensatory mutations and interbreed, the gene expression in hybrids might be disturbed, leading to sterility or unviability.

The Bateson-Dobzhansky-Muller model of genetic incompatibilities. From: Wikipedia.

Sterile Males

A recent study in the journal Genome Research applied this reasoning to hybrids between Pied Flycatcher (Ficedula hypoleuca) and Collared Flycatcher (F. albicollis). These two species diverged about one million years ago and interbreed in several locations, including the Swedish island of Öland (where the group of Anna Qvarnström has been monitoring the breeding populations for numerous years). Previous work showed that male hybrids are infertile due to the production of abnormal sperm cells. Could male sterility be the result of disrupted gene expression due to mismatches between cis- and trans-regulatory elements? To answer this question, the researchers took a closer look at gene expression patterns in five Pied Flycatchers, five Collared Flycatchers and three natural hybrids.

The analyses focused on misexpression in hybrids, which can be detected by gene expression levels in hybrids that are either higher or lower than any of the parental species. The researchers reported “evidence for abundant hybrid misexpression in heart, kidney, and liver but not in brain or testis.” In addition, more detailed analyses of genes involved in spermatogenesis did not reveal misexpression in hybrids. All in all, this study could not provide evidence that disrupted gene expression in the testis causes sterility in hybrid males. However, the high levels of misexpression in other tissues could contribute to lower hybrid fitness in other ways.

Typical sperm from a collared flycatcher (a) and a pied flycatcher (b), compared to abnormal sperm from two hybrid flycatchers, indicated by arrows (c-f). From: Ålund et al. (2013) Biology Letters.

Evolution at Two Levels

Although the testis showed no clear signs of misexpression in hybrids, this tissue did experience the highest level of divergence in gene expression between Pied and Collared Flycatcher. More research will be needed to unravel the exact changes in gene expression and their contribution to male sterility, but it seems unlikely that mismatches between cis- and trans-regulatory elements play a major role.

Despite the “negative” result, this study nicely highlights the potential involvement of regulatory changes in evolution and the formation of new species. In 1975, Mary-Claire King and A. C. Wilson already drew attention to the contrast between evolution at the sequence level and changes in patterns of gene expression. Focusing on human evolution, they noted that “a relatively small number of genetic changes in systems controlling the expression of genes may account for the major organismal differences between humans and chimpanzee.” At the time, we did not have the methods to explore how regulatory changes shape evolutionary trajectories. The development of new techniques, such as RNAseq, provide exciting opportunities to understand how changes in gene expression contribute to the origin of new species. What a wonderful time to be an evolutionary biologist.

References

Mugal, C.F., Wang, M., Backström, N., Wheatcroft, D., Ålund, M., Sémon, M., McFarlane, S.E., Dutoit, L., Qvarnström, A. & Ellegren, H. (2020). Tissue-specific patterns of regulatory changes underlying gene expression differences among Ficedula flycatchers and their naturally occurring F1 hybrids. Genome Research, 30(12), 1727-1739.

Featured image: Collared Flycatcher (Ficedula albicollis) © Andrej Chudy | Wikimedia Commons

Integrative taxonomy of the Lesser Short-toed Lark and Sand Lark species complex

The combination of genetic and non-genetic data points to four distinct species.

The advent of genetic – and later genomic – data turned out to be a double-edged sword for taxonomists. On the one hand, DNA sequences allow researchers to discriminate between morphologically similar species. On the other hand, the ability to detect ever more fine-scaled genetic differentiation between populations complicates the drawing of species boundaries. Several species delimitation programs using molecular data have been developed, but it remains a daunting task to translate the output of these programs into clear taxonomic arrangements. Jeet Sukumaran and Lacey Knowles nicely described this issue in a PNAS paper: “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.” In other words, genetic patterns will need to be corroborated by non-genetic data.

Five Lark Lineages

Several months ago, I covered a molecular study on the Lesser Short-toed Lark (Alaudala rufescens) and Sand Lark (A. raytal) species complex (see this blog post). The genetic analyses pointed to five genetic lineages that could be classified into four distinct species. Indeed, the researchers wrote that “our results call for a taxonomic revision, and we tentatively suggest that at least four species should be recognized, although we stress the need for an approach integrating molecular, morphological and other data that are not yet available.” A follow-up study in the journal Molecular Phylogenetics and Evolution provides these missing data, using plumage patterns, biometrics, songs, geographical distributions and bioclimatic factors to evaluate the genetic patterns.

A slightly more elaborate genetic analysis uncovered the same five lineages as the previous study. In addition, the species delimitation program STACEY suggested that four lineages were sufficiently divergent to warrant a species status, namely the heinei clade, the raytal clade, the rufescens clade and the cheleensis + leucophaea clade (see figure below). But what about the non-genetic data? The researchers performed several detailed analyses and an exhaustive overview of the results is not feasible within the scope of a short blog post. So, I will try to summarize the main findings below:

• The five lineages could not be separated by plumage. This is probably a consequence of the convergent evolution due to adaptation to a similar habitats.
• Classification analyses based on the wing, tail and bill lengths discriminated between all clades, except for the cheleensis and leucophaea clades. Several individuals from these groups were misclassified.
• Song characteristics were significantly different between the five clades, although the songs of cheleensis and leucophaea seemed to show a clinal pattern.
• All five lineages occur in open habitats with scant vegetation, but there appear to be some differences in habitat preferences.
• Bioclimatic parameters, such as rainfall and temperature, could discriminate between the different lineages.

Genetic analyses indicated five distinct clades. Do they all represent different species? From: Alström et al. (2021) Molecular Phylogenetics and Evolution.

Integrative Taxonomy

Based on these patterns, the researchers concluded that “the rufescens, heinei and raytal clades were unanimously supported as independent lineages by mtDNA, morphology and bioacoustics as well as by the STACEY multilocus analysis. The raytal clade was also supported by its unique habitat. The combined cheleensis and leucophaea clade was also supported by the same datasets.” The latter two clades could not be confidently separated, because they showed clinal variation in several traits. The proposed taxonomy thus includes four species:

• Lesser Short-toed Lark (A. rufescens)
• Heine’s Short-toed Lark (A. heinei)
• Asian Short-toed Lark (A. cheleensis)
• Sand Lark (A. raytal)

This study nicely illustrates the use of multiple data sources to inform taxonomic decisions (an approach known as integrative taxonomy). It is interesting to see how the genomic revolution has drawn attention to the taxonomic importance of non-genetic data, such as morphology, behavior and bioacoustics. Several authors have highlighted this perspective. I recently argued that genomics provides another line of evidence in the pluralistic approach to species classification (see this book chapter). Similarly, Carlos Daniel Cadena and Felipe Zapata called for the integration of genomic and phenotypic data in avian taxonomy (see this paper). The development of new genetic techniques is bringing us back to the basics.

References

Alström, P., van Linschooten, J., Donald, P. F., Sundev, G., Mohammadi, Z., Ghorbani, F., Shafaeipour, A., van den Berg, A., Robb, M., Aliabadian, M., Wei, C., Lei, F., Oxelman, B. & Olsson, U. (2021). Multiple species delimitation approaches applied to the avian lark genus Alaudala. Molecular Phylogenetics and Evolution, 154, 106994.

Featured image: Lesser Short-toed Lark (A. rufescens) © Juan Emilio | Wikimedia Commons

More markers, more power? Genomic analyses uncover fine-scale population structure in Philippine Broadbills

Ornithologists reconstruct the evolutionary history of several island populations.

Scientists love a good acronym. A recent study counted more than one million unique acronyms in papers published between 1950 and 2019, but just over 2,000 (0.2%) were used regularly. You can find some clever ones here, including BIGASS (Bright Infrared Galaxy All Sky Survey) and Gandalf (Gas AND Absorption Line Fitting algorithm). Ornithologists working in Asia might be familiar with the abbreviation PAIC, which stands for Pleistocene Aggregate Islands Complexes. This acronym refers to groups of islands that were connected by land bridges during the Pleistocene when sea levels were lower. The avifauna of the Philippine Archipelago seems to adhere to the PAIC model with islands complexes from different PAICs showing clear genetic divergence (see for example this study by Peter Hosner and his colleagues). However, the evolutionary history of bird populations within a single PAIC remains largely unknown. In a recent paper in the Biological Journal of the Linnean Society, researchers addressed this knowledge gap and took a closer look at the Philippine broadbills (genus Sarcophanops) of the Greater Mindanao PAIC.

Genetic Patterns

Luke Campillo and his colleagues collected samples from the Wattled Broadbill (S. steerii) and the Visayan Broadbill (S. samarensis). Genetic analyses – based on thousands of genetic markers – revealed a deep split between both species. A similar pattern emerged in a previous study using mitochondrial DNA. The researchers attributed these findings to the habitat unsuitability of the Leyte Gulf during the Pleistocene, which prevented birds from the northern and southern islands from mixing.

Apart from this deep split, the genetic analyses pointed to fine-scale diversification within the Visayan Broadbills, separating the populations from the islands Samar/Leyte and Bohol. The authors speculate that “rising sea levels at the end of the Pleistocene would have isolated Bohol first, whereas prolonged connectivity between Samar and Leyte could have promoted gene flow, thus obscuring population genetic effects of inter-island diversification.”

The genome-wide markers clearly differentiated between the two species: Wattled Broadbill (in yellow) and Visayan Broadbill (in blue). Within the latter species, further diversification between islands became apparent. Adapted from: Campillo et al. (2020) Biological Journal of the Linnean Society.

Genomic Power

The population structure within the Visayan Broadbill was not apparent in the mitochondrial DNA, highlighting the power of genome-wide markers to detect subtle signatures of population diversification. A few years ago, I covered this recent genomic development in a book chapter with several colleagues, writing that “genomic data has increased the potential for fine-scale resolution of population structure and determination of population boundaries and population membership.” However, this increase in genomic power can complicate analyses because populations tend to fall on a continuum from isolation to panmixia. Delineating populations and drawing species limits with genomic can become a daunting task. It will be interesting to follow how the genetic patterns in this study will impact the taxonomy of Philippine broadbills. Is the fine-scale population structure in the Visayan Broadbill large enough to justify subspecies or not?

References

Campillo, L. C., Manthey, J. D., Thomson, R. C., Hosner, P. A., & Moyle, R. G. (2020). Genomic differentiation in an endemic Philippine genus (Aves: Sarcophanops) owing to geographical isolation on recently disassociated islands. Biological Journal of the Linnean Society, 131(4), 814-821.

Featured image: Wattled Broadbill (Sarcophanops steerii) © Bram Demeulemeester | Flickr

Not dead yet: The decaying W-chromosome of songbirds can still acquire new genes

Researchers report the transfer of genes from the Z- to the W-chromosome.

The avian W-chromosome is slowly decaying. This female-specific chromosome (males have two Z-chromosomes) has lost almost 90 percent of its gene content and accumulated large stretches of nonsensical repeated sequences. The few genes that still reside on the W-chromosome play a role in cellular housekeeping or are involved in female-specific processes, such as the development of ovaries. It thus seems that this chromosome is destined to keep degenerating, losing more and more genes over time. However, a recent study in the journal Genes reported the transfer of several genes from the Z-chromosome to the W-chromosome. Could there still be hope for the W-chromosome?

Duplication and Deletion

While exploring the genomes of several birds-of-paradise, including the Raggiana Bird-of-paradise (Paradisaea raggiana) and the Red Bird-of-paradise (P.rubra) , Luohao Xu and his colleagues noticed something odd. A genomic region on the Z-chromosome showed unusual high sequencing coverage in females. Because females only have one Z-chromosome, you would expect less sequences in your data to map to this chromosome. Why did this specific region exhibit such high coverage? One explanation could be that the region has been duplicated, resulting in twice as many sequences mapping to it. Since this pattern was only apparent in females, the researchers suggested that this duplicated region ended up on the female-specific W-chromosome.

A closer look at the duplicated region revealed that it was about 700,000 DNA-letters long, whereas the original region on the Z-chromosome spanned 1.3 million DNA-letters. One section of the region on the W-chromosome was thus deleted, removing five complete and two partial genes. An additional two genes – ANXA1 and ALDH1A1 – survived the deletion event and were thus successfully transferred from the Z-chromosome to the W-chromosome. One of these genes (ANXA1) is active in the ovaries and might thus be preserved on the W-chromosome because of its female-specific function.

The high sequencing coverage (top graph) and elevated heterozygosity (middle graph) in females pointed to the transfer of genes from the Z-chromosome to the W-chromosome. A subsequent deletion removed several of the transferred genes (bottom figure). From: Xu et al. (2020) Genes.

Transposable Elements?

Next, the researchers repeated their analyses for a handful of other songbird species. They found similar patterns in the Medium Ground Finch (Geospiza fortis) and the Great Tit (Parus major), where other genes moved from the Z-chromosome to the W-chromosome. The relatively large sizes of the transferred sections suggest the involvement of transposable elements which are known to move large regions across the genome. More detailed sequence analyses will be needed to unravel the details of these transposition events. Whatever the mechanism, this study nicely shows that the degenerating W-chromosome can still acquire new genes.

References

Xu, L., Irestedt, M., & Zhou, Q. (2020). Sequence transpositions restore genes on the highly degenerated W chromosomes of songbirds. Genes, 11(11), 1267.

Featured image: Raggiana bird-of-paradise (Paradisaea raggiana) © David J. Stang | Wikimedia Commons

A small genomic region explains the plumage differences between Townsend’s and Hermit Warbler

Three pigmentation genes might contribute to reproductive isolation.

If I had a dollar (or euro) for every time I read “hybrid zones are natural laboratories” in a paper, I could probably sequence a fair number of bird genomes. This popular phrase can be traced back to a classic paper by Godfrey Hewitt: “Hybrid zones-natural laboratories for evolutionary studies“. And it is certainly true. Hybrid zones are extremely useful settings to learn more about the evolutionary process. Moreover, because of the recombination of different genomic regions in hybrids, it is sometimes possible to uncover the genes underlying certain traits. This approach has been successful in finding “migration genes” in the Willow Warbler (Phylloscopus trochilus) and “plumage genes” in Vermivora warblers. A recent study in the journal Evolution Letters relied on a hybrid zone between Townsend’s Warbler (Setophaga townsendi) and Hermit Warbler (S. occidentalis) to identify the genetic underpinnings of several plumage traits.

Three Genes

Silu Wang and her colleagues quantified plumage patterns in 265 individuals. They focused on seven traits: (1) cheek coloration, (2) crown coloration, (3) throat bib darkening, (4) throat bib intensity, (5) extent of breast yellow, (6) presence of black streaks on the flank, and (7) intensity of green chroma on the back. Next, the researchers performed a genome-wide association study (GWAS) to determine which genetic variants correspond to particular traits. The analyses revealed that a single variant was significantly associated with the colors of the cheek, crown and flank. This variant is located in an intron of the RALY-gene, which is known to be involved in the yellow versus black pigmentation of mice and quail. In addition, two other pigmentation genes can be found in the same region: ASIP (influences skin pigmentation in vertebrates) and EIF2S2 (associated with human skin pigmentation). How these three genes work together is still unclear, but they might function as a “super-gene” (see this blog post for more on this topic).

Location of the hybrid zone (yellow) between Townsend’s Warbler (blue) and Hermit Warbler (purple), and an overview of the different plumage traits investigated in this study. From: Wang et al. (2020) Evolution Letters.

Reproductive Isolation

Next, the researchers used the genomic data to pinpoint differentiated sections in the genome that might be involved in reproductive isolation between these warblers. This search indicated four highly differentiated genomic regions, located on chromosomes 1A, 5, 20 and the Z-chromosome. Interestingly, the region on chromosome 20 corresponds to the location of the three pigmentation genes from the GWAS. This finding suggests that the ASIP-RALY region is involved in maintaining species-specific differences and preventing these warblers from merging into one species.

The exact mechanism of reproductive isolation remains to be determined. It could be that the ASIP-RALY region facilitates assortative mating (i.e. choosing a partner that looks like you). However, a recent simulation study suggested that assortative mating alone is insufficient to stabilize hybrid zones, some degree of postzygotic selection is needed. Another possibility is that the ASIP-RALY region contributes to lower fitness in hybrids. The patchy plumage patterns of hybrids might be a disadvantage in territorial disputes, complicating a hybrids’ attempt to secure a good territory. Exciting avenues for further research, showing how genomic analyses can generate hypotheses to be tested in the field.

Exploring genomic landscape of differentiation with different genomic datasets revealed several highly differentiated regions (highlighted with red dots), including the section with the three pigmentation genes. From: Wang et al. (2020) Evolution Letters.

References

Wang, S., Rohwer, S., de Zwaan, D. R., Toews, D. P., Lovette, I. J., Mackenzie, J., & Irwin, D. (2020). Selection on a small genomic region underpins differentiation in multiple color traits between two warbler species. Evolution Letters, 4(6), 502-515.

Featured image: Townsend’s Warbler (Setophaga townsendi) © Alan Vernon | Wikimedia Commons

This paper has been added to the Parulidae page.

Rapid evolution of sexual dimorphism in island populations of the Sulawesi Babbler

Stronger intraspecific competition on islands might explain this finding.

A few weeks ago, I wrote about the molecular underpinnings of sexual dimorphism in birds (see this blog post). In most species where males and females look different, the dimorphism is very obvious. Think of the extravagant tail feathers of the male peacock (genus Pavo) compared to the dull brown female. In some species, however, the differences between males and females are more subtle and easily missed by the casual observer. For example, in descriptions of the bird family Pellorneidae (the jungle babblers), you will often read that the sexes are similar. But a closer look at these inconspicuous birds might reveal cryptic sexual dimorphism. Indeed, a recent study in the journal Biotropica uncovered subtle morphological differences between males and females of the Sulawesi Babbler (Pellorneum celebense).

Clustering

Fionn Ó Marcaigh and his colleagues examined the morphology of birds captured on the southeast peninsula of Sulawesi and on the smaller islands of Kabaena, Muna, and Buton. They applied a cluster algorithm to determine if the birds could be sorted into different subgroups based on subtle morphological differences. This approach of unsupervised clustering is well suited for detecting sexual dimorphism in body size for monochromatic bird species. The analysis separated the sampled birds into two groups that corresponded to males and females (confirmed with molecular sexing). Male babblers were consistently larger than females. Convincing evidence of sexual dimorphism in the Sulawesi Babbler.

The clustering algorithm identified two main clusters that correspond to males (green) and females (red). From: Ó Marcaigh et al. (2020). Biotropica.

Competition

The researchers also noticed that “island birds appeared more strongly dimorphic than their mainland counterparts in each of our five morphological traits.” These islands became isolated within the last 20,000 years, suggesting very rapid evolution of sexual dimorphism in the Sulawesi Babbler. The selection pressures responsible for these fast changes are probably related to intraspecific competition (i.e. between individuals of the same species). On islands, species can often occur in higher densities because there is less competition with other species. However, these higher densities might result in more fierce competition between members of the same species, potentially culminating in sexual dimorphism when males and females adapt to different ecological niches. An interesting phenomenon on the islands that Alfred Russell Wallace already described as “anomalous”. Who knows what other discoveries await us on Sulawesi?

Sexual dimorphism was more pronounced on the islands compared to the mainland, as illustrated by the diverging lines in these graphs (green = males, red = females). From: Ó Marcaigh et al. (2020). Biotropica.

References

Ó Marcaigh, F., Kelly, D. J., Analuddin, K., Karya, A., Lawless, N., & Marples, N. M. (2021). Cryptic sexual dimorphism reveals differing selection pressures on continental islands. Biotropica, 53(1), 121-129.

Featured image: Sulawesi Babbler (Pellorneum celebense) © Trinity College Dublin

The genomics of being an owl

The search for candidate genes leads to a surprising hypothesis.

Owls are beautifully adapted for a predatory lifestyle in the dark. Their big eyes contain a duplex retina that is dominated by rods, the photoreceptors that are sensitive to light. The asymmetrical position of their ears and their flat facial disk give the owls a superior sense of hearing. And their soft feathers ensure a silent flight, allowing owls to sneak up on unsuspecting prey. The morphological adaptations of these nightly birds are well-studied, but the genetic basis of these traits remains largely unknown. In a recent Genome Biology and Evolution paper, Pamela Espíndola-Hernández and her colleagues used a genomic approach to identify the genes underlying these adaptations.

Substitutions

The researchers compared the genomes of eleven owl species with nine other bird species. At the base of the owl-clade, they counted the number of nonsynonymous and synonymous substitutions. Nonsynonymous substitutions lead to a change in the protein sequence (i.e. another amino acid) and are often subjected to natural selection. Synonymous substitutions do not change the protein sequence due to the redundancy in the genetic code (see this blog post for more details on the genetic code). Because these synonymous changes to not affect the protein sequence, they are generally not picked up by natural selection. By estimating the ratio of nonsynonymous (dN) to synonymous (dS) substitutions in a gene, evolutionary biologists can detect genes under positive selection. A dN/dS ratio bigger than 1 corresponds to more nonsynonymous substitutions in a gene and points to strong positive selection.

Using this approach, the researchers were able to create a list of candidate genes subjected to positive selection in the owl genomes. After correcting for the multiple statistical tests, 22 candidate genes remained. A functional analysis of these genes revealed that they were mostly related to “detection of stimulus involved in sensory perception.” This result points to genes involved in the auditory and visual adaptations of owls. Among others, we come across the genes TMC2, which is involved in the workings of cochlear hair cells of the inner ear, and PPEF2, which is expressed specifically in photoreceptors. Interesting targets for further research.

An overview of several candidate genes and their functional pathways. These networks highlight genes involved in vision and chromosome condensation.

Light-collecting Lenses

The discovery of genes involved in vision and hearing were expected, but the analyses also uncovered another set of genes were under positive selection: those involved in chromosome condensation. This finding suggests that owls might have evolved a special type of DNA packaging in the retina, similar to what has been reported in nocturnal mammals. In most eukaryotic cells, the condensed DNA (i.e. heterochromatin) is located at the nuclear periphery and the lightly packaged DNA (i.e. euchromatin) is found at the nuclear interior. In the rods of nocturnal animals, however, this pattern is reversed, which turns the rod nuclei into light-collecting lenses. Computer simulations showed that columns of such nuclei channel light efficiently toward the light-sensing rods. Whether the same mechanism applies to the eyes of owls remains to be determined, but is certainly an exciting hypothesis to test. This result highlights the value of genome-wide quests for candidate genes, which can lead to surprising insights or new research lines.

The different arrangement of DNA in the cells of nocturnal mammals (figure K) might channel light more efficiently to the light-sensitive rods in the eye. From: Solovei et al. (2009) Cell.

References

Espíndola-Hernández, P., Mueller, J. C., Carrete, M., Boerno, S., & Kempenaers, B. (2020). Genomic evidence for sensorial adaptations to a nocturnal predatory lifestyle in owls. Genome Biology and Evolution, 12(10), 1895-1908.

Featured image: Eurasian Eagle-Owl (Bubo bubo) © Rhododendrites | Wikimedia Commons