bioRxiv Science⌕ Search

Biology subjects

Mila, B.

Publications and source records attributed to Mila, B..

13 recordsLinked to original sources

Song as a behavioural pre-mating barrier in early population divergence: Insights from the Canary Islands Chaffinch

Acoustic signaling is key to individual and species recognition, playing a major role in sexual and social communication. Since reproductive isolation is often maintained through pre-mating mechanisms, song can be an early isolating trait leading to assortative mating, promoting reproductive divergence, and potentially contributing to speciation. However, whether song differences alone are sufficient to prevent interbreeding or if other traits also contribute, remains a matter of debate. Playback experiments provide a more direct way to test the role of song as a reproductive barrier. Here, we use playback experiments to test the hypothesis that song acts as a pre-mating barrier in two recently diverged populations of an island passerine, the Canary Islands Chaffinch (Fringilla canariensis palmae), which inhabit ecologically distinct laurel and pine forests within the island of La Palma. Assuming that male song has diverged in the two habitats, we tested if territorial males from a given habitat responded differently to songs from intruding males from their own habitat or from the other habitat type, using a closely related mainland species as a control. We found that probability of response was weaker to songs of the closely related species and to the different-habitat birds than to songs of the same-habitat birds, but differences for the latter were weak. The intensity of response followed the same pattern. Overall, song divergence between laurel and pine forest chaffinches does not appear strong enough to cause clear behavioural discrimination against individuals from the alternative habitat. Other factors such as morphological and ecological divergence associated with adaptation to local resources might better explain population differentiation. However, testing female responses will be essential to determine whether songs convey lineage-specific information that may elicit assortative mating.

evolutionary biology↗

Genomics of speciation in a great speciator (Aves: Zosterops) reveals the roles of both natural and sexual selection

Examining patterns of differentiation among lineage pairs at different stages of the speciation continuum can help disentangle the effects of linked and divergent selection, and identify lineage-specific targets of selection that may act as barrier loci during speciation. Here, we developed this approach using genomic data from a set of African and Indian Ocean belonging to the Zosteropidae family, commonly referred to as a "Great Speciator". We sampled a divergence continuum aiming to identify candidate barrier loci in phenotypically, genetically distinct, and parapatrically distributed, forms from a species complex, through comparisons with closely related species. Using three independent approaches, we showed that divergence at selected loci between geographic forms is mainly concentrated on the Z chromosome, unless forms differ in their ecologies. Functional annotation revealed that genes linked to song formation and immunity could be involved in reproductive isolation between forms only separated by physical barriers, while it is mostly genes related to adaptation to local conditions, morphology, and song behaviour that may explain reproductive isolation between forms with different ecologies, highlighting a role for combined effects of natural and sexual selection in driving the evolution of reproductive barriers in this rapidly speciating lineage

genomics↗

The acoustic adaptation hypothesis across terrestrial vertebrates: a meta-analysis

Acoustic communication plays a prominent role in various ecological and evolutionary processes involving social interactions. The properties of acoustic signals are thought to be influenced not only by the interaction between signaller and receiver but also by the acoustic characteristics of the environment through which the signal is transmitted. This conjecture forms the core of the so-called "acoustic adaptation hypothesis" (AAH), which posits that vegetation structure affects frequency and temporal parameters of acoustic signals emitted by a signaller as a function of their acoustic degradation properties. Specifically, animals in densely vegetated closed habitats are expected to produce longer acoustic signals with lower repetition rates and lower frequencies (minimum, mean, maximum, and peak) compared to the ones inhabiting less vegetated open habitats. To date, this hypothesis has received mixed results, with the level of support depending on the taxonomic group and the methodology used. We conducted a systematic literature search of empirical studies testing for an effect of vegetation structure on acoustic signalling and assessed the generality of the AAH using a meta-analytic approach based on 371 effect sizes from 75 studies and 57 taxa encompassing birds, mammals and amphibians. Overall, our results do not provide consistent support for the AAH, neither in within-species comparisons (suggesting no overall phenotypically plastic response of acoustic signalling to vegetation structure) nor in among-species comparisons (suggesting no overall evolutionary response). However, when considering birds only, we found a weak support for the AAH in within-species comparisons, which was mainly driven by studies that measured frequency bandwidth, suggesting that this variable may exhibit a phenotypically plastic response to vegetation structure. For among-species comparisons in birds, we also found support for the AAH, but this effect was not significant after excluding comparative studies that did not account for phylogenetic non-independence. Collectively, our synthesis does not support a universal role of vegetation structure in the evolution of acoustic communication. We highlight the need for more empirical work on currently under-studied taxa such as amphibians, mammals, and insects. Furthermore, we propose a framework for future research on the AAH. We specifically advocate for a more detailed and quantitative characterization of habitats to identify frequencies with the highest detection probability and to determine if frequencies with greater detection distances are preferentially used. Finally, we stress that empirical tests of the AAH should focus on signals which are selected for increased transmission distance.

evolutionary biology↗

Unravelling species demographic responses to local and global past ecological disruptions using whole-genome sequencing in volcanic oceanic island organisms

Disentangling the effects of ecological disruptions operating at different spatial and temporal scales in shaping past species demography is particularly important in the current context of rapid environmental changes driven by both local and regional factors. We argue that volcanic oceanic islands provide useful settings to study the influence of past ecological disruptions operating at local and regional scales on population demographic histories. We investigate potential drivers of past population dynamics for three closely related species of passerine birds from two volcanic oceanic islands, Reunion and Mauritius (Mascarene archipelago), with distinct volcanic history. Using ABC and PSMC inferences from complete genomes, we reconstructed the demographic history of the Reunion Grey White-eye (Zosterops borbonicus (Pennant, 1781)), the Reunion Olive White-eye (Z. olivaceus (Linnaeus, 1766)), and the Mauritius Grey White-eye (Z. mauritianus (Gmelin, 1789)), and searched for possible causes underlying similarities or differences between species living on the same or different islands. Both demographic inferences strongly support ancient and long-term expansions in all species. They also reveal different trajectories between species inhabiting different islands, but consistent demographic trajectories in species or populations from the same island. Species from Reunion appear to have experienced synchronous reductions in population size during the Last Glacial Maximum, a trend not seen in the Mauritian species. Overall, this study suggests that local events may have played a role in shaping population trajectories of these island species. It also highlights the potential of our conceptual framework to disentangle the effects of local and regional drivers on past species demography and long-term population processes.

evolutionary biology↗

The hidden structural variability in avian genomes

Structural variants (SVs) are DNA mutations that can have relevant effects at micro- and macro-evolutionary scales. The detection of SVs is largely limited by the type and quality of sequencing technologies adopted, therefore genetic variability linked to SVs may remain undiscovered, especially in complex repetitive genomic regions. In this study, we used a combination of long-read and linked-read genome assemblies to investigate the occurrence of insertions and deletions across the chromosomes of 14 species of birds-of-paradise and two species of estrildid finches including highly repetitive W chromosomes. The species sampling encompasses most genera and representatives from all major clades of birds-of-paradise, allowing comparisons between individuals of the same species, genus, and family. We found the highest densities of SVs to be located on the microchromosomes and on the female-specific W chromosome. Genome assemblies of multiple individuals from the same species allowed us to compare the levels of genetic variability linked to SVs and single nucleotide polymorphisms (SNPs) on the W and other chromosomes. Our results demonstrate that the avian W chromosome harbours more genetic variability than previously thought and that its structure is shaped by the continuous accumulation and turnover of transposable element insertions, especially endogenous retroviruses.

evolutionary biology↗

Chromosome-level genome assembly of the common chaffinch (Aves: Fringilla coelebs): a valuable resource for evolutionary biology

The common chaffinch, Fringilla coelebs, is one of the most common, widespread and well-studied passerines in Europe, with a broad distribution encompassing Western Europe and parts of Asia, North Africa and the Macaronesian archipelagos. We present a high-quality genome assembly of the common chaffinch generated using Illumina shotgun sequencing in combination with Chicago and Hi-C libraries. The final genome is a 994.87 Mb chromosome-level assembly, with 98% of the sequence data located in chromosome scaffolds and a N50 statistic of 69.73 Mb. Our genome assembly shows high completeness, with a complete BUSCO score of 93.9% using the avian dataset. Around 7.8 % of the genome contains interspersed repetitive elements. The structural annotation yielded 17,703 genes, 86.5% of which have a functional annotation, including 7,827 complete universal single-copy orthologs out of 8,338 genes represented in the BUSCO avian data set. This new annotated genome assembly will be a valuable resource as a reference for comparative and population genomic analyses of passerine, avian and vertebrate evolution.

evolutionary biology↗

The island rule explains consistent patterns of body size evolution across terrestrial vertebrates

Island faunas can be characterized by gigantism in small animals and dwarfism in large animals, but the extent to which this so-called island rule provides a general explanation for evolutionary trajectories on islands remains contentious. Here we use a phylogenetic meta-analysis to assess patterns and drivers of body size evolution across a global sample of paired island-mainland populations of terrestrial vertebrates. We show that island rule effects are widespread in mammals, birds and reptiles, but less evident in amphibians, which mostly tend towards gigantism. We also found that the magnitude of insular dwarfism and gigantism is mediated by climate as well as island size and isolation, with more pronounced effects in smaller, more remote islands for mammals and reptiles. We conclude that the island rule is pervasive across vertebrates, but that the implications for body size evolution are nuanced and depend on an array of context-dependent ecological pressures and environmental conditions.

ecology↗

Endemic island songbirds as windows into evolution in small effective population sizes

Due to their limited ranges and inherent isolation, island species have long been recognized as crucial systems for tackling a range of evolutionary questions, including in the early study of speciation [1,2]. Such species have been less studied in the understanding of the evolutionary forces driving DNA sequence evolution. Island species usually have lower census population sizes (N) than continental species and, supposedly, lower effective population sizes (Ne). Given that both the rates of change caused by genetic drift and by selection are dependent upon Ne, island species are theoretically expected to exhibit (i) lower genetic diversity, (ii) less effective natural selection against slightly deleterious mutations [3,4], and (iii) a lower rate of adaptive evolution [5-8, see also Note S1]. Here, we have used a large set of newly sequenced and published whole genome sequences of Passerida bird species or subspecies (14 insular and 11 continental) to test these predictions. We empirically confirm that island species exhibit lower census size and Ne, supporting the hypothesis that the smaller area available on islands constrains the upper bound of Ne. In the insular species, we find significantly lower nucleotide diversity in coding regions, higher ratios of non-synonymous to synonymous polymorphisms, and lower adaptive substitution rates. Our results provide robust evidence that the lower Ne experienced by island species has affected both the ability of natural selection to efficiently remove weakly deleterious mutations and also the adaptive potential of island species, therefore providing considerable empirical support for the nearly neutral theory. We discuss the implications for both evolutionary and conservation biology.

evolutionary biology↗

A bird’s white-eye shot: looking down on a new avian sex chromosome evolution

AO_SCPCAPBSTRACTC_SCPCAPChromosomal organization is relatively stable among avian species, especially with regards to sex chromosomes. Members of the large Sylvioidea clade however have a pair of neo-sex chromosomes which is unique to this clade and originate from a parallel translocation of a region of the ancestral 4A chromosome on both W and Z chromosomes. Here, we took advantage of this unusual event to study the early stages of sex chromosome evolution. To do so, we sequenced a female (ZW) of two Sylvioidea species, a Zosterops borbonicus and a Z. pallidus. Then, we organized the Z. borbonicus scaffolds along chromosomes and annotated genes. Molecular phylogenetic dating under various methods and calibration sets confidently confirmed the recent diversification of the genus Zosterops (1-3.5 million years ago), thus representing one of the most exceptional rates of diversification among vertebrates. We then combined genomic coverage comparisons of five males and seven females, and homology with the zebra finch genome (Taeniopygia guttata) to identify sex chromosome scaffolds, as well as the candidate chromosome breakpoints for the two translocation events. We observed reduced levels of within-species diversity in both translocated regions and, as expected, even more so on the neoW chromosome. In order to compare the rates of molecular evolution in genomic regions of the autosomal-to-sex transitions, we then estimated the ratios of non-synonymous to synonymous polymorphisms ({pi}N/{pi}S) and substitutions (dN/dS). Based on both ratios, no or little contrast between autosomal and Z genes was observed, thus representing a very different outcome than the higher ratios observed at the neoW genes. In addition, we report significant changes in base composition content for translocated regions on the W and Z chromosomes and a large accumulation of transposable elements (TE) on the newly W region. Our results revealed contrasted signals of molecular evolution changes associated to these autosome-to-sex transitions, with congruent signals of a W chromosome degeneration yet a surprisingly weak support for a fast-Z effect.

evolutionary biology↗

Change in sexual signaling traits outruns morphological divergence in a recent avian radiation across an ecological gradient

The relative roles of natural and sexual selection in promoting evolutionary lineage divergence remains controversial and difficult to assess in natural systems. Local adaptation through natural selection is known to play a central role in adaptive radiations, yet secondary sexual traits can vary widely among species in recent radiations, suggesting that sexual selection may also be important in the early stages of speciation. Here we compare rates of divergence in ecologically relevant traits (morphology) and sexually selected signaling traits (coloration) relative to neutral structure in genome-wide molecular markers, and examine patterns of variation in sexual dichromatism to understand the roles of natural and sexual selection in the diversification of the songbird genus Junco (Aves: Passerellidae). Juncos include divergent lineages in Central America and several dark-eyed junco (J. hyemalis) lineages that diversified recently as the group recolonized North America following the last glacial maximum (c.a. 18,000 years ago). We found an accelerated rate of divergence in sexually selected characters relative to ecologically relevant traits. Moreover, a synthetic index of sexual dichromatism comparable across lineages revealed a positive relationship between the degree of color divergence and the strength of sexual selection, especially when controlling for neutral genetic distance. We also found a positive correlation between dichromatism and latitude, which coincides with the latitudinal pattern of decreasing lineage age but also with a steep ecological gradient. Finally, we detected an association between outlier loci potentially under selection and both sexual dichromatism and latitude of breeding range. These results suggest that the joint effects of sexual and ecological selection have played a role in the junco radiation and can be important in the early stages of lineage formation.

evolutionary biology↗

Local adaptation and sexual selection drive intra-island diversification in a songbird lineage: differential divergence in autosomes and sex chromosomes.

Recently diverged taxa showing marked phenotypic and ecological diversity are optimal systems to test the relative importance of two major evolutionary mechanisms, adaptation to local ecological conditions by natural selection, or mechanisms of reproductive isolation such as assortative mating mediated by sexually selected mating signals or post-zygotic incompatibilities. Whereas local adaptation is expected to affect many loci throughout the genome, traits acting as mating signals are expected to be located on sex chromosomes and have a simple genetic basis. We used genome-wide markers to test these predictions in Reunion Islands gray-white eye (Zosterops borbonicus), which has recently diversified into five distinct plumage forms. Two of them correspond to a polymorphic highland population that is separated by a steep ecological gradient from three distinct lowland forms that show narrow contact zones in plumage color traits, yet no association with environmental variables. An analysis of population structure using genome-wide SNP loci revealed two major clades corresponding to highland and lowland forms, respectively, with the latter separated further into three independent lineages corresponding to plumage forms. Coalescent tests of alternative demographic scenarios provided support for divergence of highland and lowland lineages with an intensification of gene flow in the last 60,000 years. Landscapes of genomic variation revealed that signatures of selection associated with elevation are found at multiple regions across the genome, whereas most loci associated with the lowland forms are located on the Z sex chromosome. A gene ontology analysis identified TYRP1, a Z-linked color gene, as a likely candidate locus underlying color variation among lowland forms. Our results are consistent with the role of natural selection in driving the divergence of locally adapted highland populations, and the role of sexual selection in differentiating lowland forms through reproductive isolation mechanisms, showing that both modes of lineage divergence can take place at very small geographic scales in birds.

evolutionary biology↗

A role for differential gene regulation in the rapid diversification of melanic plumage coloration in the dark-eyed junco (Junco hyemalis)

Color plays a prominent role in reproductive isolation, therefore understanding the proximal basis of pigmentation can provide insight into speciation. Subspecies of the dark-eyed junco (Junco hyemalis) have evolved marked differences in plumage coloration since the Last Glacial Maximum, yet whether color differences are caused by mutations in coding regions of expressed genes or are instead the result of regulatory differences remains unknown. To address this question, we studied the pigment composition and the genetic basis of coloration in two divergent subspecies, the slate-colored and Oregon juncos. We used HPLC and light microscopy to investigate pigment composition and deposition in feathers from four body areas. We then used RNAseq to compare the relative roles of differential gene expression in developing feathers and sequence divergence in transcribed loci under common garden conditions. Junco feathers differed in eumelanin and pheomelanin content and distribution. Within subspecies, in lighter feathers melanin synthesis genes were downregulated (including PMEL, TYR, TYRP1, OCA2, MLANA), ASIP was upregulated. Feathers from different body regions also showed differential expression of HOX and Wnt genes. Feathers from the same body regions that differed in color between the two subspecies showed differential expression of ASIP and three other genes (MFSD12, KCNJ13, HAND2) associated with pigmentation in other taxa. Sequence variation in the expressed genes was not related to color differences. Our findings support the hypothesis that differential regulation of a few genes can account for marked differences in coloration, a mechanism that may underlie the rapid diversification of juncos.

evolutionary biology↗

Genome-wide signals of drift and local adaptation during rapid lineage divergence in a songbird

The formation of independent evolutionary lineages involves neutral and selective factors, and understanding their relative roles in population divergence is a fundamental goal of speciation research. Correlations between allele frequencies and environmental variability can reveal the role of selection, yet the relative contribution of drift can be difficult to establish. Recently diversified systems such as that of the Oregon junco (Aves: Emberizidae) of western North America provide ideal scenarios to apply genetic-environment association analyses (GEA) while controlling for population structure. Genome-wide SNP loci analyses revealed marked genetic structure consisting of differentiated populations in isolated, dry southern mountain ranges, and more admixed recently expanded populations in humid northern latitudes. We used correlations between genomic and environmental variance to test for three specific modes of evolutionary divergence: (i) drift in geographic isolation, (ii) differentiation along continuous selective gradients, and (iii) isolation by adaptation. We found evidence of strong drift in southern mountains, but also signals of local adaptation in several populations, driven by temperature, precipitation, elevation and vegetation, especially when controlling for population history. We identified numerous variants under selection scattered across the genome, suggesting that local adaptation can promote rapid differentiation over short periods when acting over multiple independent loci.

evolutionary biology↗