Ecological niche divergence or ecological niche partitioning in a widespread Neotropical bird lineage.

Ecological niche divergence is generally considered to be a facet of evolution that may accompany geographic isolation and diversification in allopatry, contributing to species' evolutionary distinctiveness through time. The null expectation for any two diverging species in geographic isolation is that of niche conservatism, wherein populations do not rapidly shift to or adapt to novel environments. Here, I test ecological niche divergence for a widespread, pan-American lineage, the avian genus of martins (Progne). The genus Progne includes migrant and resident species, as well as geographically restricted taxa and widespread, intercontinentally distributed taxa, thus providing an ideal group in which to study the nature of niche divergence within a broad geographic mosaic. I obtained distributional information for the genus from publicly available databases and created ecological niche models for each species to create pairwise comparisons of environmental space. I combined these data with the most up-to-date phylogeny of Progne currently available to examine the patterns of niche evolution within the genus. I found limited evidence for niche divergence across the breeding distributions of Progne, and much stronger support for niche conservatism with patterns of niche partitioning. The ancestral Progne had a relatively broad ecological niche, like extant basal Progne lineages, and several geographically localized descendant species occupy only portions of this larger ancestral niche. I recovered strong evidence of breeding niche divergence for four of 36 taxon pairs but only one of these divergent pairs involved two widespread species (Southern Martin P. elegans vs. Gray-breasted Martin P. chalybea). Potential niche expansion from the ancestral species was observed in the most wide-ranging present-day species, namely the North American Purple Martin P. subis and P. chalybea. I analyzed populations of P. subis separately, as a microcosm of Progne evolution, and again found only limited evidence of niche divergence. This study adds to the mounting evidence for niche conservatism as a dominant feature of diversifying lineages, and sheds light on the ways in which apparently divergent niches may arise through allopatry while not involving any true niche shifts through evolutionary time. Even taxa that appear unique in terms of habitat or behavior may not be diversifying with respect to their ecological niches, but merely partitioning ancestral niches among descendant taxa.

Ecological niche divergence or ecological niche partitioning in a widespread Neotropical bird lineage.

Ecological niche divergence is generally considered to be a facet of evolution that may accompany geographic isolation and diversification in allopatry, contributing to species' evolutionary distinctiveness through time. The null expectation for any two diverging species in geographic isolation is that of niche conservatism, wherein populations do not rapidly shift to or adapt to novel environments. Here, I test ecological niche divergence for a widespread, pan-American lineage, the avian genus of martins (Progne). Despite containing species with distributions that go from continent-spanning to locally endemic, I found limited evidence for niche divergence across the breeding distributions of Progne, and much stronger support for niche conservatism with patterns of niche partitioning. The ancestral Progne had a relatively broad ecological niche, similar to extant basal Progne lineages, and several geographically localized descendant species occupy only portions of the larger ancestral Progne niche. I recovered strong evidence of breeding niche divergence for four of 36 taxon pairs but only one of these divergent pairs involved two widespread, continental species (Southern Martin P. elegans vs. Gray-breasted Martin P. chalybea). Potential niche expansion from the ancestral species was observed in the most wide-ranging present-day species, namely the North American Purple Martin P. subis and P. chalybea. I analyzed populations of P. subis separately, as a microcosm of Progne evolution, and again found only limited evidence of niche divergence. This study adds to the mounting evidence for niche conservatism as a dominant feature of diversifying lineages. Even taxa that appear unique in terms of habitat or behavior may still not be diversifying with respect to their ecological niches, but merely partitioning ancestral niches among descendant taxa.

A new hybrid incompatibility locus between Drosophila melanogaster and Drosophila sechellia.

Despite the fundamental importance of hybrid incompatibilities to the process of speciation, there are few cases where the evolution and genetic architecture of hybrid incompatibilities are understood. One of the longest studied hybrid incompatibilities causes F1 hybrid male inviability in crosses between Drosophila melanogaster females and males from the Drosophila simulans clade of species-Drosophila simulans, Drosophila mauritiana, and Drosophila sechellia. Here, we discover dramatic differences in the manifestation of this lethal hybrid incompatibility among the D. simulans clade of species. In particular, F1 hybrid males between D. melanogaster and D. sechellia are resistant to hybrid rescue through RNAi knockdown of an essential hybrid incompatibility gene. To understand the genetic basis of this inter-species difference in hybrid rescue, we developed a triple-hybrid mapping method. Our results show that 2 discrete large effect loci and many dispersed small effect changes across the genome underlie D. sechellia aversion to hybrid rescue. The large effect loci encompass a known incompatibility gene Lethal hybrid rescue (Lhr) and previously unknown factor, Sechellia aversion to hybrid rescue (Satyr). These results show that the genetic architecture of F1 hybrid male inviability is overlapping but not identical in the 3 inter-species crosses. Our results raise questions about whether new hybrid incompatibility genes can integrate into an existing hybrid incompatibility thus increasing in complexity over time, or if the continued evolution of genes can gradually strengthen an existing hybrid incompatibility.

What constitutes a community? A co-occurrence exploration of the Costa Rican avifauna.

The concept of a "community" as a form of organization for natural biological systems is both widespread and widely accepted within the ecological and biological sciences. Communities have been defined as groups of organisms that interact in ways that denote interdependence between individuals and taxa (e.g. as defined by "food webs") but they have also been defined as groups of co-occurring organisms that are assumed to interact by virtue of their shared spatiotemporal existence. The latter definition has been debated and challenged in the literature, with mounting evidence for co-occurrence being more indicative of coincident ecological niches in space and time rather than being evidence of ecological interaction or dependency. Using a dataset of 460 Costa Rican bird species divided into breeding and non-breeding season datasets, we empirically demonstrate the ways in which co-occurrence can create illusory communities based on similar occupied ecological niches and similar patterns of co-occurrence at different times of year. We discuss the importance of discerning coincidental co-occurrence from true ecological interactions that would manifest a true community, and further address the importance of differentiating communities of co-occurrence from communities of demonstrable ecological interaction. While co-occurrence is a necessary aspect of interspecific interactions, we discuss and demonstrate here that such co-occurrence does not make a community, nor should explicit patterns of co-occurrence be seen as evidence for evolutionarily important ecological interactions.

Interspecific hybridization explains rapid gorget colour divergence in Heliodoxa hummingbirds (Aves: Trochilidae).

Hybridization is a known source of morphological, functional and communicative signal novelty in many organisms. Although diverse mechanisms of established novel ornamentation have been identified in natural populations, we lack an understanding of hybridization effects across levels of biological scales and upon phylogenies. Hummingbirds display diverse structural colours resulting from coherent light scattering by feather nanostructures. Given the complex relationship between feather nanostructures and the colours they produce, intermediate coloration does not necessarily imply intermediate nanostructures. Here, we characterize nanostructural, ecological and genetic inputs in a distinctive Heliodoxa hummingbird from the foothills of eastern Peru. Genetically, this individual is closely allied with Heliodoxa branickii and Heliodoxa gularis, but it is not identical to either when nuclear data are assessed. Elevated interspecific heterozygosity further suggests it is a hybrid backcross to H. branickii. Electron microscopy and spectrophotometry of this unique individual reveal key nanostructural differences underlying its distinct gorget colour, confirmed by optical modelling. Phylogenetic comparative analysis suggests that the observed gorget coloration divergence from both parentals to this individual would take 6.6-10 My to evolve at the current rate within a single hummingbird lineage. These results emphasize the mosaic nature of hybridization and suggest that hybridization may contribute to the structural colour diversity found across hummingbirds.

Climatic refugia and reduced extinction correlate with underdispersion in mammals and birds in Africa.

Macroevolutionary patterns, often inferred from metrics of community relatedness, are often used to ascertain major evolutionary processes shaping communities. These patterns have been shown to be informative of biogeographic barriers, of habitat suitability and invasibility (especially with regard to environmental filtering), and of regions that function as evolutionary cradles (i.e., sources of diversification) or museums (i.e., regions of reduced extinction). Here, we analyzed continental datasets of mammal and bird distributions to identify primary drivers of community evolution on the African continent for mostly endothermic vertebrates. We find that underdispersion (i.e., relatively low phylogenetic diversity compared to species richness) closely correlates with specific ecoregions that have been identified as climatic refugia in the literature, regardless of whether these specific regions have been touted as cradles or museums. Using theoretical models of identical communities that differ only with respect to extinction rates, we find that even small suppressions of extinction rates can result in underdispersed communities, supporting the hypothesis that climatic stability can lead to underdispersion. We posit that large-scale patterns of under- and overdispersion between regions of similar species richness are more reflective of a particular region's extinction potential, and that the very nature of refugia can lead to underdispersion via the steady accumulation of species richness through diversification within the same ecoregion during climatic cycles. Thus, patterns of environmental filtering can be obfuscated by environments that coincide with biogeographic refugia, and considerations of regional biogeographic history are paramount for inferring macroevolutionary processes.

Hierarchical analyses of avian community biogeography in the Afromontane highlands.

The Afromontane mountains are a complex series of highlands that have intermittently been connected by habitat corridors during climatic cycles, resulting in a mosaic of range disjunctions and allospecies complexes in the present day. Patterns of community relatedness between geographic regions are often determined through single-species analyses or spatial analyses of diversity and nestedness at the species level. To understand patterns of Afromontane community evolution and to assess the effects of taxonomy on our understanding of biogeographic patterns, I concatenated three lists of Afromontane bird taxa divided into five taxonomic hierarchies. These lists were converted into a presence-absence matrix across 42 montane regions and analyzed using a variety of clustering techniques based on a replicable coding pipeline. I used these lists and methods to determine patterns of relatedness between montane blocks, to assess the consistency with which biogeographic regions were recovered, and to shed light on the patterns of connectivity within the Afromontane region. My results reaffirm the distinctiveness of many biogeographic regions (e.g., the Cameroon Highlands) while also clarifying regional relationships and the presence of 'transition zones' between regions. Differences between lists illustrated how our understanding of taxonomy and distribution in the Afromontane highlands can also change our understanding of Afromontane biogeography. Most notably, I found evidence for an Expanded Eastern Arc that included the Eastern Arc Mountains and highlands in Malawi, Mozambique, and Zimbabwe. This study presents a rigorous yet easily adjustable pipeline for studying regional biogeography from multiple taxonomic perspectives using both traditional and novel approaches.

Dispersal ability correlates with range size in Amazonian habitat-restricted birds.

Understanding how species attain their geographical distributions and identifying traits correlated with range size are important objectives in biogeography, evolutionary biology and biodiversity conservation. Despite much effort, results have been varied and general trends have been slow to emerge. Studying species pools that occupy specific habitats, rather than clades or large groupings of species occupying diverse habitats, may better identify ranges size correlates and be more informative for conservation programmes in a rapidly changing world. We evaluated correlations between a set of organismal traits and range size in bird species from Amazonian white-sand ecosystems. We assessed if results are consistent when using different data sources for phylogenetic and range hypotheses. We found that dispersal ability, as measured by the hand-wing index, was correlated with range size in both white-sand birds and their non-white-sand sister taxa. White-sand birds had smaller ranges on average than their sister taxa. The results were similar and robust to the different data sources. Our results suggest that the patchiness of white-sand ecosystems limits species' ability to reach new habitat islands and establish new populations.

Acknowledging uncertainty in evolutionary reconstructions of ecological niches.

Reconstructing ecological niche evolution can provide insight into the biogeography and diversification of evolving lineages. However, comparative phylogenetic methods may infer the history of ecological niche evolution inaccurately because (a) species' niches are often poorly characterized; and (b) phylogenetic comparative methods rely on niche summary statistics rather than full estimates of species' environmental tolerances. Here, we propose a new framework for coding ecological niches and reconstructing their evolution that explicitly acknowledges and incorporates the uncertainty introduced by incomplete niche characterization. Then, we modify existing ancestral state inference methods to leverage full estimates of environmental tolerances. We provide a worked empirical example of our method, investigating ecological niche evolution in the New World orioles (Aves: Passeriformes: Icterus spp.). Temperature and precipitation tolerances were generally broad and conserved among orioles, with niche reduction and specialization limited to a few terminal branches. Tools for performing these reconstructions are available in a new R package called nichevol.

Roles of C/EBP class bZip proteins in the growth and cell competition of Rp ('Minute') mutants in Drosophila.

Reduced copy number of ribosomal protein (Rp) genes adversely affects both flies and mammals. Xrp1 encodes a reportedly Drosophila-specific AT-hook, bZIP protein responsible for many of the effects including the elimination of Rp mutant cells by competition with wild type cells. Irbp18, an evolutionarily conserved bZIP gene, heterodimerizes with Xrp1 and with another bZip protein, dATF4. We show that Irbp18 is required for the effects of Xrp1, whereas dATF4 does not share the same phenotype, indicating that Xrp1/Irbp18 is the complex active in Rp mutant cells, independently of other complexes that share Irbp18. Xrp1 and Irbp18 transcripts and proteins are upregulated in Rp mutant cells by auto-regulatory expression that depends on the Xrp1 DNA binding domains and is necessary for cell competition. We show that Xrp1 is conserved beyond Drosophila, although under positive selection for rapid evolution, and that at least one human bZip protein can similarly affect Drosophila development.

Recurrent Losses and Rapid Evolution of the Condensin II Complex in Insects.

Condensins play a crucial role in the organization of genetic material by compacting and disentangling chromosomes. Based on studies in a few model organisms, the condensins I and II complexes are considered to have distinct functions, with the condensin II complex playing a role in meiosis and somatic pairing of homologous chromosomes in Drosophila. Intriguingly, the Cap-G2 subunit of condensin II is absent in Drosophila melanogaster, and this loss may be related to the high levels of chromosome pairing seen in flies. Here, we find that all three non-SMC subunits of condensin II (Cap-G2, Cap-D3, and Cap-H2) have been repeatedly and independently lost in taxa representing multiple insect orders, with some taxa lacking all three. We also find that all non-Dipteran insects display near-uniform low-pairing levels regardless of their condensin II complex composition, suggesting that some key aspects of genome organization are robust to condensin II subunit losses. Finally, we observe consistent signatures of positive selection in condensin subunits across flies and mammals. These findings suggest that these ancient complexes are far more evolutionarily labile than previously suspected, and are at the crossroads of several forms of genomic conflicts. Our results raise fundamental questions about the specific functions of the two condensin complexes in taxa that have experienced subunit losses, and open the door to further investigations to elucidate the diversity of molecular mechanisms that underlie genome organization across various life forms.

Reconstructing Ecological Niche Evolution When Niches Are Incompletely Characterized.

Evolutionary dynamics of abiotic ecological niches across phylogenetic history can shed light on large-scale biogeographic patterns, macroevolutionary rate shifts, and the relative ability of lineages to respond to global change. An unresolved question is how best to represent and reconstruct evolution of these complex traits at coarse spatial scales through time. Studies have approached this question by integrating phylogenetic comparative methods with niche estimates inferred from correlative and other models. However, methods for estimating niches often produce incomplete characterizations, as they are inferred from present-day distributions that may be limited in full expression of the fundamental ecological niche by biotic interactions, dispersal limitations, and the existing set of environmental conditions. Here, we test whether incomplete niche characterizations inherent in most estimates of species' niches bias phylogenetic reconstructions of niche evolution, using simulations of virtual species with known niches. Results establish that incompletely characterized niches inflate estimates of evolutionary change and lead to error in ancestral state reconstructions. Our analyses also provide a potential mechanism to explain the frequent observation that maximum thermal tolerances are more conserved than minimum thermal tolerances: populations and species experience more spatial variation in minimum temperature than in maximum temperature across their distributions and, consequently, may experience stronger diversifying selection for cold tolerance.

Predictable invasion dynamics in North American populations of the Eurasian collared dove Streptopelia decaocto.

Species invasions represent a significant dimension of global change yet the dynamics of invasions remain poorly understood and are considered rather unpredictable. We explored interannual dynamics of the invasion process in the Eurasian collared dove (Streptopelia decaocto) and tested whether the advance of the invasion front of the species in North America relates to centrality (versus peripherality) within its estimated fundamental ecological niche. We used ecological niche modelling approaches to estimate the dimensions of the fundamental ecological niche on the Old World distribution of the species, and then transferred that model to the New World as measures of centrality versus peripherality within the niche for the species. Although our hypothesis was that the invasion front would advance faster over more favourable (i.e. more central) conditions, the reverse was the case: the invasion expanded faster in areas presenting less favourable (i.e. more peripheral) conditions for the species as it advanced across North America. This result offers a first view of a predictive approach to the dynamics of species' invasions, and thereby has relevant implications for the management of invasive species, as such a predictive understanding would allow better anticipation of coming steps and advances in the progress of invasions, important to designing and guiding effective remediation and mitigation efforts.

Parallel Evolution of Sperm Hyper-Activation Ca2+ Channels.

Sperm hyper-activation is a dramatic change in sperm behavior where mature sperm burst into a final sprint in the race to the egg. The mechanism of sperm hyper-activation in many metazoans, including humans, consists of a jolt of Ca2+ into the sperm flagellum via CatSper ion channels. Surprisingly, all nine CatSper genes have been independently lost in several animal lineages. In Drosophila, sperm hyper-activation is performed through the cooption of the polycystic kidney disease 2 (pkd2) Ca2+ channel. The parallels between CatSpers in primates and pkd2 in Drosophila provide a unique opportunity to examine the molecular evolution of the sperm hyper-activation machinery in two independent, nonhomologous calcium channels separated by > 500 million years of divergence. Here, we use a comprehensive phylogenomic approach to investigate the selective pressures on these sperm hyper-activation channels. First, we find that the entire CatSper complex evolves rapidly under recurrent positive selection in primates. Second, we find that pkd2 has parallel patterns of adaptive evolution in Drosophila. Third, we show that this adaptive evolution of pkd2 is driven by its role in sperm hyper-activation. These patterns of selection suggest that the evolution of the sperm hyper-activation machinery is driven by sexual conflict with antagonistic ligands that modulate channel activity. Together, our results add sperm hyper-activation channels to the class of fast evolving reproductive proteins and provide insights into the mechanisms used by the sexes to manipulate sperm behavior.

A genomic approach to identify hybrid incompatibility genes.

Uncovering the genetic and molecular basis of barriers to gene flow between populations is key to understanding how new species are born. Intrinsic postzygotic reproductive barriers such as hybrid sterility and hybrid inviability are caused by deleterious genetic interactions known as hybrid incompatibilities. The difficulty in identifying these hybrid incompatibility genes remains a rate-limiting step in our understanding of the molecular basis of speciation. We recently described how whole genome sequencing can be applied to identify hybrid incompatibility genes, even from genetically terminal hybrids. Using this approach, we discovered a new hybrid incompatibility gene, gfzf, between Drosophila melanogaster and Drosophila simulans, and found that it plays an essential role in cell cycle regulation. Here, we discuss the history of the hunt for incompatibility genes between these species, discuss the molecular roles of gfzf in cell cycle regulation, and explore how intragenomic conflict drives the evolution of fundamental cellular mechanisms that lead to the developmental arrest of hybrids.

An essential cell cycle regulation gene causes hybrid inviability in Drosophila.

Speciation, the process by which new biological species arise, involves the evolution of reproductive barriers, such as hybrid sterility or inviability between populations. However, identifying hybrid incompatibility genes remains a key obstacle in understanding the molecular basis of reproductive isolation. We devised a genomic screen, which identified a cell cycle-regulation gene as the cause of male inviability in hybrids resulting from a cross between Drosophila melanogaster and D. simulans. Ablation of the D. simulans allele of this gene is sufficient to rescue the adult viability of hybrid males. This dominantly acting cell cycle regulator causes mitotic arrest and, thereby, inviability of male hybrid larvae. Our genomic method provides a facile means to accelerate the identification of hybrid incompatibility genes in other model and nonmodel systems.