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The perfect storm: Gene tree estimation error, incomplete lineage sorting, and ancient gene flow explain the most recalcitrant ancient angiosperm clade, Malpighiales
<p>The genomic revolution offers renewed hope of resolving rapid radiations in the Tree of Life. The development of the multispecies coalescent (MSC) model and improved gene tree estimation methods can better accommodate gene tree heterogeneity caused by incomplete lineage sorting (ILS) and gene tree estimation error stemming from the short internal branches. However, the relative influence of these factors in species tree inference is not well understood. Using anchored hybrid enrichment, we generated a data set including 423 single-copy loci from 64 taxa representing 39 families to infer the species tree of the flowering plant order Malpighiales. This order includes nine of the top ten most unstable nodes in angiosperms, which have been hypothesized to arise from the rapid radiation during the Cretaceous. Here, we show that coalescent-based methods do not resolve the backbone of Malpighiales and concatenation methods yield inconsistent estimations, providing evidence that gene tree heterogeneity is high in this clade. Despite high levels of ILS and gene tree estimation error, our simulations demonstrate that these two factors alone are insufficient to explain the lack of resolution in this order. To explore this further, we examined triplet frequencies among empirical gene trees and discovered some of them deviated significantly from those attributed to ILS and estimation error, suggesting gene flow as an additional and previously unappreciated phenomenon promoting gene tree variation in Malpighiales. Finally, we applied a novel method to quantify the relative contribution of these three primary sources of gene tree heterogeneity and demonstrated that ILS, gene tree estimation error, and gene flow contributed to 15%, 52%, and 32% of the variation, respectively. Together, our results suggest that a perfect storm of factors likely influence this lack of resolution, and further indicate that recalcitrant phylogenetic relationships like the backbone of Malpighiales may be better represented as phylogenetic networks. Thus, reducing such groups solely to existing models that adhere strictly to bifurcating trees greatly oversimplifies reality, and obscures our ability to more clearly discern the process of evolution.</p>
Data from: Integrating incomplete fossils by isolating conflictive signal in saturated and non-independent morphological characters
Morphological characters are indispensable in phylogenetic analyses for understanding the pattern, process, and tempo of evolution. If characters are independent and free of systematic errors, then combining as many different kinds of characters as are available will result in the best-supported phylogenetic hypotheses. But since morphological characters are subject to natural selection for function and arise from the expression of developmental pathways, they may not be independent, a situation that may amplify any underlying homoplasy. Here, we use new dental and multi-locus genetic data from bats (Mammalia: Chiroptera) to quantify saturation and similarity in morphological characters and introduce two likelihood-based approaches to identify strongly conflicting characters and integrate morphological and molecular data. We implement these methods to analyze the phylogeny of incomplete Miocene fossils in the radiation of Phyllostomidae (New World Leaf-nosed Bats), perhaps the most ecologically diverse family of living mammals. Morphological characters produced trees incongruent with molecular phylogenies, were saturated, and showed rates of change higher than most molecular substitution rates. Dental characters encoded variation similar to that in other morphological characters, while molecular characters encoded highly dissimilar variation in comparison. Saturation and high rates of change indicate randomization of phylogenetic signal in the morphological data, and extensive similarity suggests characters are non-independent and errors are amplified. To integrate the morphological data into tree building while accounting for homoplasy, we used statistical molecular scaffolds and combined phylogenetic analyses excluding a small subset of strongly conflicting dental characters. The phylogenies revealed the Miocene nectar-feeding †Palynephyllum nests within the crown nectar-feeding South American subfamily Lonchophyllinae, while the Miocene genus †Notonycteris is sister to the extant carnivorous Vampyrum. These relationships imply new calibration points for timing of radiation of the ecologically diverse Phyllostomidae.
Data from: Evaluating summary statistics used to test for incomplete lineage sorting: mito-nuclear discordance in the reef sponge Callyspongia vaginalis
Conflicting patterns of population differentiation between the mitochondrial and nuclear genomes (mito-nuclear discordance) have become increasingly evident as multilocus datasets have become easier to generate. Incomplete lineage sorting (ILS) of nucDNA is often implicated as the cause of such discordance, stemming from the large effective population size of nucDNA relative to mtDNA. However, selection, sex-biased dispersal, and historical demography can also lead to mito-nuclear discordance. Here we compare patterns of genetic diversity and subdivision for six nuclear protein-coding gene regions to those for mtDNA in a common Caribbean coral reef sponge, Callyspongia vaginalis, along the Florida reef tract. We also evaluated a suite of summary statistics to determine which are effective metrics for comparing empirical and simulated data when testing drivers of mito-nuclear discordance in a statistical framework. While earlier work revealed three divergent and geographically subdivided mtDNA COI haplotypes separated by 2.4% sequence divergence, nuclear alleles were admixed with respect to mitochondrial clade and geography. Bayesian analysis showed substitution rates for the nuclear loci were up to 7 times faster than for mitochondrial COI. Coalescent simulations and neutrality tests suggested that mito-nuclear discordance in C. vaginalis is not the result of ILS in the nucDNA or selection on the mtDNA but is more likely caused by changes in population size. Sperm-mediated gene flow may also influence patterns of population subdivision in the nucDNA.
Data from: Occasional males in parthenogenetic populations of Asobara japonica (Hymenoptera: Braconidae): low Wolbachia titer or incomplete co-adaptation?
Wolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts. Some populations of the parasitoid wasp Asobara japonica are infected with Wolbachia and reproduce parthenogenetically, while other populations are not infected and reproduce sexually. Wolbachia infected A. japonica females regularly produce small numbers of male offspring. Because all females in the field are infected and infected females are not capable of sexual reproduction, male production seems to be maladaptive. We investigated why these females nevertheless produce males. We tested three hypotheses: high rearing temperatures could result in higher offspring sex ratios (more males), low Wolbachia titer of the mother could lead to higher offspring sex ratios and/or the Wolbachia infection is of relatively recent origin and not enough time has passed to allow complete co-adaptation between Wolbachia and host. Thirty-three percent of the Wolbachia infected females produced males and 56% of these males were also infected with Wolbachia. Neither offspring sex ratio nor male infection frequency were significantly affected by rearing temperature or Wolbachia concentration of the mother. The mitochondrial DNA sequence of one of the uninfected populations was identical to that of two of the infected populations. Therefore, the initial Wolbachia infection of A. japonica must have occurred recently. Mitochondrial sequence variation among infected populations suggests that the spread of Wolbachia through the host populations involved horizontal transmission. We conclude that the occasional male production by Wolbachia infected females is most likely a maladaptive side-effect of incomplete co-evolution between symbiont and host in this relatively young infection.
Data from: Mouse fitness measures reveal incomplete functional redundancy of Hox paralogous group 1 proteins
Here we assess the fitness consequences of the replacement of the Hoxa1 coding region with its paralog Hoxb1 in mice (Mus musculus) residing in semi-natural enclosures. Previously, this Hoxa1B1 swap was reported as resulting in no discernible embryonic or physiological phenotype (i.e., functionally redundant), despite the 51% amino acid sequence differences between these two Hox proteins. Within heterozygous breeding cages no differences in litter size nor deviations from Mendelian genotypic expectations were observed in the outbred progeny; however, within semi-natural population enclosures mice homozygous for the Hoxa1B1 swap were out-reproduced by controls resulting in the mutant allele being only 87.5% as frequent as the control in offspring born within enclosures. Specifically, Hoxa1B1 founders produced only 77.9% as many offspring relative to controls, as measured by homozygous pups, and a 22.1% deficiency of heterozygous offspring was also observed. These data suggest that Hoxa1 and Hoxb1 have diverged in function through either sub- or neo-functionalization and that the HoxA1 and HoxB1 proteins are not mutually interchangeable when expressed from the Hoxa1 locus. The fitness assays conducted under naturalistic conditions in this study have provided an ultimate-level assessment of the postulated equivalence of competing alleles. Characterization of these differences has provided greater understanding of the forces shaping the maintenance and diversifications of Hox genes as well as other paralogous genes. This fitness assay approach can be applied to any genetic manipulation and often provides the most sensitive way to detect functional differences.
Data from: Incomplete datasets obscure associations between traits affecting dispersal ability and geographic range size of reef fishes in the Tropical Eastern Pacific
Dispersal is thought to be an important process determining range size, especially for species in highly spatially structured habitats, such as tropical reef fishes. Despite intensive research efforts, there is conflicting evidence about the role of dispersal on determining range size. We hypothesize that traits related to dispersal drive range sizes, but that complete and comprehensive datasets are essential for detecting relationships between species' dispersal ability and range size. We investigate the roles of six traits affecting several stages of dispersal (adult mobility, spawning mode, pelagic larval duration (PLD), body size, aggregation behaviour and circadian activity), in explaining range size variation of reef fishes in the Tropical Eastern Pacific (TEP). All traits, except for PLD (148 species), had data for all 497 species in the region. Using a series of models, we investigated which traits were associated with large range sizes, when analysing all TEP species or only species with PLD data. Furthermore, using null models, we analysed whether the PLD-subset is representative of the regional species pool. Several traits affecting dispersal ability were strongly associated with range size, although these relationships could not be detected when using the PLD-data subset. Pelagic spawners (allowing for passive egg dispersal) had on average 56% larger range sizes than non-pelagic spawners. Species with medium or high adult mobility had on average a 25% or 33% larger range, respectively, than species with low mobility. Null models showed that the PLD-subset was non-representative of the regional species pool, explaining why model outcomes using the PLD-subset differed from the ones based on the complete dataset. Our results show that in the TEP, traits affecting dispersal ability are important in explaining range size variation. Using a regionally complete dataset was crucial for detecting the theoretically expected, but so far empirically unresolved, relationship between dispersal and range size.
Data from: Testing the role of mating preference in a case of incomplete ecological speciation with gene flow
Mating preference can evolve as a side effect of ecological adaptation and simultaneously contribute to speciation in certain scenarios. However, theoretical predictions have been difficult to test experimentally because there has not been any simple way to relate empirical and theoretical parameters. Recently, it has been shown that the r coefficient and other statistics can be used to estimate mating preference in wild-captured mating pairs. In the present work we use these estimators to test whether mating preference has significantly increased in a context favorable for ecological divergence. We perform the study using two groups of samples from populations of the marine gastropod Littorina saxatilis: 1) a group of bimodal populations affected by ecological divergence, and 2) a group of unimodal populations. The results show that mating preference (unlike the trait affected by the preference) does not increase when two ecotypes meet and mate in sympatry, which suggests that mating preference must be controlled by strong stabilizing natural selection, and/or limited by mating cost. This would suggest that mating preference would rarely contribute to speciation under the face of gene flow in these ecotypes.
Data from: Weak disruptive selection and incomplete phenotypic divergence in two classic examples of sympatric speciation: Cameroon crater lake cichlids
Recent documentation of a few compelling examples of sympatric speciation led to a proliferation of theoretical models. Unfortunately, plausible examples from nature have rarely been used to test model predictions, such as the initial presence of strong disruptive selection. Here I estimated the form and strength of selection in two classic examples of sympatric speciation: radiations of Cameroon cichlids restricted to lakes Barombi Mbo and Ejagham. I measured five functional traits and relative growth rates in over 500 individuals within incipient species complexes from each lake. Disruptive selection was prevalent in both groups on single and multivariate trait axes, but weak relative to stabilizing selection on other traits and most published estimates of disruptive selection. Furthermore, despite genetic structure, assortative mating, and bimodal species-diagnostic coloration, trait distributions were unimodal in both species complexes, indicating the earliest stages of speciation. Long waiting times or incomplete sympatric speciation may result when disruptive selection is initially weak. Alternatively, I present evidence of additional constraints in both species complexes, including weak linkage between coloration and morphology, reduced morphological variance aligned with nonlinear selection surfaces, and minimal ecological divergence. While other species within these radiations show complete phenotypic separation, morphological and ecological divergence in these species complexes may be slow or incomplete outside optimal parameter ranges, in contrast to rapid divergence of their sexual coloration.
Data from: Forest snail faunas from Crimea (Ukraine), an isolated and incomplete Pleistocene refugium
The land snail faunas of 26 forest sites and two open rocky sites in the Crimean Mountains were sampled in 2011. Of the 40 species found within the forests (about half the known fauna of Crimea as a whole), 28 were species with wide western Palaearctic distributions, and only eight were endemic to Crimea. While there were significant differences in the faunas of different sampling areas, these seemed to be a consequence of ecological differences among them rather than a product of geographical isolation and differentiation. Endemic species were large, and not entirely restricted to forest; known endemics not found in these forests are mainly typical of more open habitats. There is no local radiation of small species living in damp forest litter, as with Leiostyla species in the Transcaucasian forest refugium, and families such as the Clausiliidae with many endemic forest species in both Transcaucasia and the Carpathians are sparsely represented. The one endemic clausiliid genus, Mentissa, occurs in open as well as in wooded habitats. The present faunas are rather poor considering the soil conditions and climate, and the forests hold widespread species often associated with open habitats elsewhere. While there is evidence that these mountains provided a refuge for many animals and plants during glacial episodes further north, the forest snail fauna suggests that full forest cover did not survive throughout the Pleistocene. Rather, the present fauna contains endemics that survived in other habitats and widespread species with good powers of passive dispersal.
Data from: Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete taxon sampling
Replicate radiations provide powerful comparative systems to address questions about the interplay between opportunity and innovation in driving episodes of diversification and the factors limiting their subsequent progression. However, such systems have been rarely documented at intercontinental scales. Here, we evaluate the hypothesis of multiple radiations in the genus Lupinus (Leguminosae), which exhibits some of the highest known rates of net diversification in plants. Given that incomplete taxon sampling, background extinction, and lineage-specific variation in diversification rates can confound macroevolutionary inferences regarding the timing and mechanisms of cladogenesis, we used Bayesian relaxed clock phylogenetic analyses as well as MEDUSA and BiSSE birth–death likelihood models of diversification, to evaluate the evolutionary patterns of lineage accumulation in Lupinus. We identified 3 significant shifts to increased rates of net diversification (r) relative to background levels in the genus (r = 0.18–0.48 lineages/myr). The primary shift occurred approximately 4.6 Ma (r = 0.48–1.76) in the montane regions of western North America, followed by a secondary shift approximately 2.7 Ma (r = 0.89–3.33) associated with range expansion and diversification of allopatrically distributed sister clades in the Mexican highlands and Andes. We also recovered evidence for a third independent shift approximately 6.5 Ma at the base of a lower elevation eastern South American grassland and campo rupestre clade (r = 0.36–1.33). Bayesian ancestral state reconstructions and BiSSE likelihood analyses of correlated diversification indicated that increased rates of speciation are strongly associated with the derived evolution of perennial life history and invasion of montane ecosystems. Although we currently lack hard evidence for "replicate adaptive radiations" in the sense of convergent morphological and ecological trajectories among species in different clades, these results are consistent with the hypothesis that iteroparity functioned as an adaptive key innovation, providing a mechanism for range expansion and rapid divergence in upper elevation regions across much of the New World.
Fig. 10. Ancestral area reconstruction for Priapulus caudatus estimated from S in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 10. Ancestral area reconstruction for Priapulus caudatus estimated from S-DIVA algorithm using ultrametric COI tree calculated in BEAST 2.4 software. Numbers at the tips of the trees correspond to the sampling locations on the map (designated as in Fig. 1). Letters represent most likely ancestral range. Sectors in circles indicate the percent of total range probability. Biogeographical regions in the map as in Piepenburg et al. (2011), Ekimova et al. (2019), Laakkonen et al. (2021).
Fig. 2 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 2. Morphology of Arctic Priapulus caudatus. A. Individual WS19002 from the intertidal of the White Sea, showing the body division into introvert (in), trunk (tr) and caudal appendage (ca). B. Frontal scanning electron microscopical (SEM) image of individual WS19002 from the White Sea showing the longitudinal rows of scalids (sc) and the pentagons of pharyngeal teeth (the first five pentagons are labelled with numbers. C. Individual XZ4889 from the Barents Sea, for abbreviations see A. D, E. Frontal view on individual XZ5288 from the Laptev Sea with light microscopy (D) and SEM (E). F. Lateral view on everted pharyngeal teeth in individual XZ5496 from the East-Siberia Sea. Pharyngeal teeth of pentagons 1 to 6 are labelled. G, H. Individual XZ5374 from the Laptev Sea, for abbreviations in G see figure A. H is a magnification showing the ring papillae (rp), posterior warts (pw) and the vesicles (ves) of the caudal appendage.
Fig. 1 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 1. Sampling locations: 1 – Northwest Atlantic (Cobscook Bay), 2 – North Sea (Scotland), 3 – North Sea (Bergen), 4 – Skagerrak (Kristineberg), 5 – Baltic Sea (Oresund), 6 – Norwegian Sea (Tromsø), 7 – Barents Sea (Dalnie Zelentsy), 8 – White Sea, 9 – Barents Sea (Russkaya Gavan), 10 – Kara Sea (Abrosimov Bay), 11 – Gulf of Ob, 12 – Laptev Sea (Severnaya Zemlya), 13 – Laptev Sea (Vilkitsky Strait), 14 – shelf of the Laptev Sea, 15 – Laptev Sea (Buor- Haya), 16 – shallow of the East Siberian Sea, 17 – East Siberian Sea (Chaunskaya Bay), 18 – Chuckchi Sea (Gerold Island), 19 – Sea of Okhotsk (Magadan), 20 – North Pacific (Kamchatka), 21 – North Pacific (Alaska). Green circles indicate individuals from GenBank, yellow circles indicate our samples. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 6. Single-gene Bayesian trees for 16S and FoxQ2 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 6. Single-gene Bayesian trees for 16S and FoxQ2 markers. Numbers above nodes indicate bootstrap values from Bayesian Interference (BI), black numbers below—posterior probabilities from Maximum Likelihood (ML), only bootstrap values> 60 are shown.
Fig. 9 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 9. Divergence time estimates from BEAST analysis for major Priapulus caudatus clades with different calibration scenarios (CS). Dates are in millions of years. Green dots indicate the main divergence nodes, orange dots show Okhotsk clade divergence node. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 7 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 7. Haplotype TCS network from COI for Priapulus caudatus (including available sequences from GenBank). Frames indicate the main haplogroups, tick marks between haplotypes indicate number of substitutions, relative size of the circles reflects the number of individuals in the haplotype. Colors indicate sample location. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 4 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 4. Distribution of five main COI clades around the studied area (including available sequences from GenBank).
Fig. 5 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 5. Right: Bayesian phylogenetic tree of Priapulus caudatus based on COI dataset (without sequences from GenBank). Numbers above nodes indicate bootstrap values from Bayesian Interference (BI), black numbers below—posterior probabilities from Maximum Likelihood (ML), only bootstrap values> 60 are shown. Blue and yellow boxes show 28S + 18S genotypes. Individuals in yellow boxes belong to the intertidal genotype, individuals in blue boxes belong to the subtidal genotype; individuals in half-yellow-half-blue boxes are heterozygotes. Asterisks mark individuals collected in the intertidal (0 m), the rest are from the subtidal (5–500 m). Left: intertidal (yellow worms) and subtidal (blue worms) populations of Priapulus caudatus. Some larvae from intertidal populations pass to the subtidal with the tide. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Fig. 3 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 3. Single-gene Bayesian trees for COI marker (including all available sequences from GenBank). Numbers above nodes indicate bootstrap values from Bayesian Interference (BI), black numbers below—posterior probabilities from Maximum Likelihood (ML), only bootstrap values> 50 are shown.
Fig. 8 in Cryptic species complex or an incomplete speciation? Phylogeographic analysis reveals an intricate Pleistocene history of Priapulus caudatus Lamarck, 1816
Fig. 8. Ultrametric COI tree calculated in BEAST 2.4 software under the Birth-Death model in 107 MCMC generations (including available sequences from GenBank). Black numbers above branches indicate millions of years (Mya); white numbers below indicate posterior probabilities. On the left side: classic subdivision of the Pliocene-Pleistocene according to Horikawa et al. (2015), M¨oller et al. (2019), and Astakhov and Semionova (2021). Grey boxes indicate glacial periods.
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These curated guides explain access requirements, typical timelines, costs, and reuse considerations for widely used research datasets.
Allen Brain Atlas
Allen Brain Atlas is an Allen Institute collection of brain map atlases, datasets, APIs, and analysis tools covering mouse, human, and non-human primate brain resources.
Annotated Behaviour and Observability Dataset (ABODe)
ABODe is a University of Edinburgh DataShare dataset for behavior classification in group-housed mice using home-cage video, identities, bounding boxes, ground-plate positions, and annotator labels.
DANDI Archive for NWB datasets
DANDI is a BRAIN Initiative archive for publishing and sharing neurophysiology data, including electrophysiology, optophysiology, and behavioral data packaged as NWB and related standards.
International Brain Laboratory public data
The International Brain Laboratory public data releases expose standardized mouse decision-making experiments, including Neuropixels recordings, widefield calcium imaging, behavior, and session metadata accessed through the ONE API.
OpenNeuro
OpenNeuro is a free, open platform for sharing neuroimaging datasets, with public search, dataset pages, and download paths for web, S3, DataLad, and the OpenNeuro CLI.