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"Passeriformes"
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Earth history and the passerine superradiation
SignificanceOur understanding of the factors that affected the diversification of passerines, the most diverse and widespread bird order (Passeriformes), is limited. Here, we reconstruct passerine evolutionary history and produce the most comprehensive time-calibrated phylogenetic hypothesis of the group using extensive sampling of the genome, complete sampling of all passerine families, and a number of vetted fossil calibration points. Our phylogenetic results refine our knowledge of passerine diversity and yield divergence dates that are consistent with the fossil record, and our macroevolutionary analyses suggest that singular events in Earth history, such as increases in Cenozoic global temperature or the colonization of new continents, were not the primary forces driving passerine diversification.
Avian diversification has been influenced by global climate change, plate tectonic movements, and mass extinction events. However, the impact of these factors on the diversification of the hyperdiverse perching birds (passerines) is unclear because family level relationships are unresolved and the timing of splitting events among lineages is uncertain. We analyzed DNA data from 4,060 nuclear loci and 137 passerine families using concatenation and coalescent approaches to infer a comprehensive phylogenetic hypothesis that clarifies relationships among all passerine families. Then, we calibrated this phylogeny using 13 fossils to examine the effects of different events in Earth history on the timing and rate of passerine diversification. Our analyses reconcile passerine diversification with the fossil and geological records; suggest that passerines originated on the Australian landmass ∼47 Ma; and show that subsequent dispersal and diversification of passerines was affected by a number of climatological and geological events, such as Oligocene glaciation and inundation of the New Zealand landmass. Although passerine diversification rates fluctuated throughout the Cenozoic, we find no link between the rate of passerine diversification and Cenozoic global temperature, and our analyses show that the increases in passerine diversification rate we observe are disconnected from the colonization of new continents. Taken together, these results suggest more complex mechanisms than temperature change or ecological opportunity have controlled macroscale patterns of passerine speciation.
Journal Article
High dispersal ability inhibits speciation in a continental radiation of passerine birds
Dispersal can stimulate speciation by facilitating geographical expansion across barriers or inhibit speciation by maintaining gene flow among populations. Therefore, the relationship between dispersal ability and speciation rates can be positive or negative. Furthermore, an ‘intermediate dispersal’ model that combines positive and negative effects predicts a unimodal relationship between dispersal and diversification. Because both dispersal ability and speciation rates are difficult to quantify, empirical evidence for the relationship between dispersal and diversification remains scarce. Using a surrogate for flight performance and a species-level DNA-based phylogeny of a large South American bird radiation (the Furnariidae), we found that lineages with higher dispersal ability experienced lower speciation rates. We propose that the degree of fragmentation or permeability of the geographical setting together with the intermediate dispersal model are crucial in reconciling previous, often contradictory findings regarding the relationship between dispersal and diversification.
Journal Article
Darwin' s Galapagos finches in modern biology
One of the classic examples of adaptive radiation under natural selection is the evolution of 15 closely related species of Darwin's finches (Passeriformes), whose primary diversity lies in the size and shape of their beaks. Since Charles Darwin and other members of the Beagle expedition collected these birds on the Galapagos Islands in 1835 and introduced them to science, they have been the subjects of intense research. Many biology textbooks use Darwin's finches to illustrate a variety of topics of evolutionary theory, such as speciation, natural selection and niche partitioning. Today, as this Theme Issue illustrates, Darwin's finches continue to be a very valuable source of biological discovery. Certain advantages of studying this group allow further breakthroughs in our understanding of changes in recent island biodiversity, mechanisms of speciation and hybridization, evolution of cognitive behaviours, principles of beak/jaw biomechanics as well as the underlying developmental genetic mechanisms in generating morphological diversity. Our objective was to bring together some of the key workers in the field of ecology and evolutionary biology who study Darwin's finches or whose studies were inspired by research on Darwin's finches. Insights provided by papers collected in this Theme Issue will be of interest to a wide audience.
Journal Article
Symmetry breaking in the embryonic skin triggers directional and sequential plumage patterning
The development of an organism involves the formation of patterns from initially homogeneous surfaces in a reproducible manner. Simulations of various theoretical models recapitulate final states of natural patterns, yet drawing testable hypotheses from those often remains difficult. Consequently, little is known about pattern-forming events. Here, we surveyed plumage patterns and their emergence in Galliformes, ratites, passerines, and penguins, together representing the three major taxa of the avian phylogeny, and built a unified model that not only reproduces final patterns but also intrinsically generates shared and varying directionality, sequence, and duration of patterning. We used in vivo and ex vivo experiments to test its parameter-based predictions. We showed that directional and sequential pattern progression depends on a species-specific prepattern: an initial break in surface symmetry launches a travelling front of sharply defined, oriented domains with self-organising capacity. This front propagates through the timely transfer of increased cell density mediated by cell proliferation, which controls overall patterning duration. These results show that universal mechanisms combining prepatterning and self-organisation govern the timely emergence of the plumage pattern in birds.
Journal Article
Species coexistence and the dynamics of phenotypic evolution in adaptive radiation
Increased trait differences among sympatric lineages of ovenbirds are explained by their greater evolutionary age compared with allopatric lineages.
Relationships strained in adaptive radiations
During adaptive radiations, species that share geographic ranges (in sympatry) have higher levels of character divergence than those that are geographically isolated (in allopatry). The traditional explanation invokes species interactions: selection favours greater divergence when there is direct competition for the same ecological niche. This has never been robustly tested at broader macroevolutionary scales, however. These authors present an extensive assessment of phenotypic divergence in the context of evolutionary time, focusing on ovenbirds, one of the most diverse families of birds in the world. Estimates of divergence in multiple genes and traits across a radiation of 350 ovenbird lineages show that the ecological or reproductive traits of coexisting species are no more divergent than those of non-interacting species, instead providing evidence that species interactions can drive widespread phenotypic convergence.
Interactions between species can promote evolutionary divergence of ecological traits and social signals
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, a process widely assumed to generate species differences in adaptive radiation
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. However, an alternative view is that lineages typically interact when relatively old
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, by which time selection for divergence is weak
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and potentially exceeded by convergent selection acting on traits mediating interspecific competition
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. Few studies have tested these contrasting predictions across large radiations, or by controlling for evolutionary time. Thus the role of species interactions in driving broad-scale patterns of trait divergence is unclear
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. Here we use phylogenetic estimates of divergence times to show that increased trait differences among coexisting lineages of ovenbirds (Furnariidae) are explained by their greater evolutionary age in relation to non-interacting lineages, and that—when these temporal biases are accounted for—the only significant effect of coexistence is convergence in a social signal (song). Our results conflict with the conventional view that coexistence promotes trait divergence among co-occurring organisms at macroevolutionary scales, and instead provide evidence that species interactions can drive phenotypic convergence across entire radiations, a pattern generally concealed by biases in age.
Journal Article
Morphologically cryptic Amazonian bird species pairs exhibit strong postzygotic reproductive isolation
We possess limited understanding of how speciation unfolds in the most species-rich region of the planet—the Amazon basin. Hybrid zones provide valuable information on the evolution of reproductive isolation, but few studies of Amazonian vertebrate hybrid zones have rigorously examined the genome-wide underpinnings of reproductive isolation. We used genome-wide genetic datasets to show that two deeply diverged, but morphologically cryptic sister species of forest understorey birds show little evidence for prezygotic reproductive isolation, but substantial postzygotic isolation. Patterns of heterozygosity and hybrid index revealed that hybrid classes with heavily recombined genomes are rare and closely match simulations with high levels of selection against hybrids. Genomic and geographical clines exhibit a remarkable similarity across loci in cline centres, and have exceptionally narrow cline widths, suggesting that postzygotic isolation is driven by genetic incompatibilities at many loci, rather than a few loci of strong effect. We propose Amazonian understorey forest birds speciate slowly via gradual accumulation of postzygotic genetic incompatibilities, with prezygotic barriers playing a less important role. Our results suggest old, cryptic Amazonian taxa classified as subspecies could have substantial postzygotic isolation deserving species recognition and that species richness is likely to be substantially underestimated in Amazonia.
Journal Article
Divergent and parallel routes of biochemical adaptation in high-altitude passerine birds from the Qinghai-Tibet Plateau
When different species experience similar selection pressures, the probability of evolving similar adaptive solutions may be influenced by legacies of evolutionary history, such as lineage-specific changes in genetic background. Here we test for adaptive convergence in hemoglobin (Hb) function among high-altitude passerine birds that are native to the Qinghai-Tibet Plateau, and we examine whether convergent increases in Hb–O₂ affinity have a similar molecular basis in different species. We documented that high-altitude parid and aegithalid species from the Qinghai-Tibet Plateau have evolved derived increases in Hb–O₂ affinity in comparison with their closest lowland relatives in East Asia. However, convergent increases in Hb–O₂ affinity and convergence in underlying functional mechanisms were seldom attributable to the same amino acid substitutions in different species. Using ancestral protein resurrection and site-directed mutagenesis, we experimentally confirmed two cases in which parallel substitutions contributed to convergent increases in Hb–O₂ affinity in codistributed high-altitude species. In one case involving the ground tit (Parus humilis) and gray-crested tit (Lophophanes dichrous), parallel amino acid replacements with affinity-enhancing effects were attributable to nonsynonymous substitutions at a CpG dinucleotide, suggesting a possible role for mutation bias in promoting recurrent changes at the same site. Overall, most altitude-related changes in Hb function were caused by divergent amino acid substitutions, and a select few were caused by parallel substitutions that produced similar phenotypic effects on the divergent genetic backgrounds of different species.
Journal Article
Species richness and morphological diversity of passerine birds
The relationship between species richness and the occupation of niche space can provide insight into the processes that shape patterns of biodiversity. For example, if species interactions constrained coexistence, one might expect tendencies toward even spacing within niche space and positive relationships between diversity and total niche volume. I use morphological diversity of passerine birds as a proxy for diet, foraging maneuvers, and foraging substrates and examine the morphological space occupied by regional and local passerine avifaunas. Although independently diversified regional faunas exhibit convergent morphology, species are clustered rather than evenly distributed, the volume of the morphological space is weakly related to number of species per taxonomic family, and morphological volume is unrelated to number of species within both regional avifaunas and local assemblages. These results seemingly contradict patterns expected when species interactions constrain regional or local diversity, and they suggest a larger role for diversification, extinction, and dispersal limitation in shaping species richness.
Journal Article
Feather moult and bird appearance are correlated with global warming over the last 200 years
Global warming alters various avian phenological processes, including advanced reproduction and migration schedules. In birds, individual appearance is largely determined by plumage, influencing, for example, bird attractiveness, social status and camouflage. Juveniles of most passerine species replace their nest-grown plumage during the first months of life, a process that is called post-juvenile feather moult. Using data from ten natural history collections, we show that the extent of the post-juvenile moult has increased significantly over the last 212 years (1805–2016), a trend that is positively correlated with the temperature of the environment. Therefore, it seems that birds replaced more feathers under warmer conditions, causing juveniles to appear more similar to adult birds. Moreover, in several species, we describe a male–female switch in the extent of moult, with females currently replacing more feathers than males compared to the past. These results demonstrate different biological responses to climate warming by different phenotypes.
Most passerine bird species replace part of their plumage within the first year of life. Here, using data from 4,012 individuals of 19 species, Kiat et al. find that the extent of post-juvenile moult has increased over the past 212 years and this correlated with the global temperature increase in this period.
Journal Article