Data from: Female-biased gape and body-size dimorphism in the New World watersnakes (tribe: Thamnophiini) oppose predictions from Rensch’s Rule
Contributors: Burbrink, Frank, Futterman, India
... Sexual size dimorphism (SSD) is ubiquitous across animals with female bias most prominent in snakes and other ectothermic organisms. To understand how SSD evolves across species, Rensch’s Rule predicts that in taxa where males are larger, SSD increases with body size. In contrast, where females are larger, SSD decreases with body size. While this rule holds for many taxa, it may be ambiguous for others, particularly ectothermic vertebrates. Importantly, this rule suggests that the outcomes of SSD over phylogenetic time scales depends on the direction of dimorphism predicated on the difference in reproductive efforts between males and females. Here we examine SSD in the context of Rensch’s Rule in Thamnophiini, the garter and waternsakes, a prominent group composing the North American snake biota. Using a dated phylogeny, measurements of gape, body and tail size, we show that these snakes do not follow Rensch’s Rule, but rather female-biased SSD increases with body size. We in turn find that this allometry is most pronounced with gape and is correlated with both neonate and litter size, suggesting that acquiring prey of increased size may be directly related to fecundity selection. These changes in SSD are not constrained to any particular clade; we find no evidence of phylogenetic shifts in those traits showing SSD. We suggest several ways forward to better understand the anatomical units of selection for SSD and modularity
Contributors: Chan, Ying-Chi, Tibbitts, T Lee, Lok, Tamar, Hassell, Chris J., Peng, He-Bo, Ma, Zhijun, Zhang, Zhengwang, Piersma, Theunis
... 1. Satellite-based technologies that track individual animal movements enable the mapping of their spatial and temporal patterns of occurrence. This is particularly useful in poorly studied or remote regions where there is a need for the rapid gathering of relevant ecological knowledge to inform management actions. One such region is East Asia, where many intertidal habitats are being degraded at unprecedented rates and shorebird populations relying on these habitats show rapid declines. 2. We examine the utility of satellite tracking to accelerate the identification of coastal sites of conservation importance in the East Asian-Australasian Flyway. In 2015–2017 we used solar-powered satellite transmitters to track the migration of 32 great knots (Calidris tenuirostris), an ‘Endangered’ shorebird species widely distributed in the Flyway and fully dependent on intertidal habitats for foraging during the non-breeding season. 3. From the great knot tracks, a total of 92 stopping sites along the Flyway were identified. Surprisingly, 63% of these sites were not known as important shorebird sites before our study; in fact, every one of the tracked individuals used sites that were previously unrecognized. 4. Site knowledge from on-ground studies in the Flyway is most complete for the Yellow Sea and generally lacking for Southeast Asia, Southern China, and Eastern Russia. 5. Policy implications: Satellite tracking highlighted coastal habitats that are potentially important for shorebirds but lack ecological information and conservation recognition, such as those in Southern China and Southeast Asia. At the same time, the distributional data of tracked individuals can direct on-ground surveys at the lesser-known sites to collect information on bird numbers and habitat characteristics. To recognize and subsequently protect valuable coastal habitats, filling knowledge gaps by integrating bird tracking with ground-based methods should be prioritized.19-Jun-2019
Data from: Verbalizing phylogenomic conflict: representation of node congruence across competing reconstructions of the neoavian explosion
Contributors: Franz, Nico M., Musher, Lukas J., Brown, Joseph W., Shizhuo, Yu, Ludäscher, Bertram
... Phylogenomic research is accelerating the publication of landmark studies that aim to resolve deep divergences of major organismal groups. Meanwhile, systems for identifying and integrating the products of phylogenomic inference–such as newly supported clade concepts–have not kept pace. However, the ability to verbalize node concept congruence and conflict across multiple, in effect simultaneously endorsed phylogenomic hypotheses, is a prerequisite for building synthetic data environments for biological systematics and other domains impacted by these conflicting inferences. Here we develop a novel solution to the conflict verbalization challenge, based on a logic representation and reasoning approach that utilizes the language of Region Connection Calculus (RCC–5) to produce consistent alignments of node concepts endorsed by incongruent phylogenomic studies. The approach employs clade concept labels to individuate concepts used by each source, even if these carry identical names. Indirect RCC–5 modeling of intensional (property-based) node concept definitions, facilitated by the local relaxation of coverage constraints, allows parent concepts to attain congruence in spite of their differentially sampled children. To demonstrate the feasibility of this approach, we align two recent phylogenomic reconstructions of higher-level avian groups that entail strong conflict in the "neoavian explosion" region. According to our representations, this conflict is constituted by 26 instances of input "whole concept" overlap. These instances are further resolvable in the output labeling schemes and visualizations as "split concepts", which provide the labels and relations needed to build truly synthetic phylogenomic data environments. Because the RCC–5 alignments fundamentally reflect the trained, logic-enabled judgments of systematic experts, future designs for such environments need to promote a culture where experts routinely assess the intensionalities of node concepts published by our peers–even and especially when we are not in agreement with each other.
Contributors: Eliason, Chad, Andersen, Michael, Hackett, Shannon
... Color is among the most striking features of organisms, varying not only in spectral properties like hue and brightness, but also in where and how it is produced on the body. Different combinations of colors on a bird’s body are important in both environmental and social contexts. Previous comparative studies have treated plumage patches individually or derived plumage complexity scores from color measurements across a bird’s body. However, these approaches do not consider the multivariate nature of plumages (allowing for plumage to evolve as a whole) or account for interpatch distances. Here, we leverage a rich toolkit used in historical biogeography to assess color pattern evolution in a cosmopolitan radiation of birds, kingfishers (Aves: Alcedinidae). We demonstrate the utility of this approach and test hypotheses about the tempo and mode of color evolution in kingfishers. Our results highlight the importance of considering interpatch distances in understanding macroevolutionary trends in color diversity and demonstrate how historical biogeography models are a useful way to model plumage color pattern evolution. Furthermore, they show that distinct color mechanisms (pigments or structural colors) spread across the body in different ways and at different rates. Specifically, net rates are higher for structural colors than pigment-based colors. Together, our study suggests a role for both development and selection in driving extraordinary color pattern diversity in kingfishers. We anticipate this approach will be useful for modeling other complex phenotypes besides color, such as parasite evolution across the body.
Contributors: Self Davies, Zoe, Spence, Andrew, Wilson, Alan
... Horse locomotion is remarkably economical. Here we measure external mechanical work of the galloping horse and relate it to published measurements of metabolic cost. Seven Thoroughbred horses were galloped (ridden) over force plates, under a racing surface. Twenty-six full strides of force data were recorded and used to calculate external mechanical work of galloping. The mean sum of decrements of mechanical energy was -876J (± 280J) per stride and increments were 2163J (± 358J) per stride as horses were accelerating. Combination with published values for internal work and metabolic costs for galloping yield an apparent muscular efficiency of 37-46% for galloping which would be reduced by energy storage in leg tendons. Knowledge about external work of galloping provides further insight into the mechanics of galloping from both an evolutionary and performance standpoint.
Data from: Restriction-site-associated DNA sequencing reveals a cryptic viburnum species on the North American coastal plain
Contributors: Spriggs, Elizabeth L., Eaton, Deren A.R., Sweeney, Patrick W., Schlutius, Caroline, Edwards, Erika J., Donoghue, Michael J.
... Species are the starting point for most studies of ecology and evolution, but the proper circumscription of species can be extremely difficult in morphologically variable lineages, and there are still few convincing examples of molecularly-informed species delimitation in plants. We focus here on the Viburnum nudum complex, a highly variable clade that is widely distributed in eastern North America. Taxonomic treatments have mostly divided this complex into northern (V. nudum var. cassinoides) and southern (V. nudum var. nudum) entities, but additional names have been proposed. We used multiple lines of evidence, including RADseq, morphological, and geographic data, to test how many independently evolving lineages exist within the V. nudum complex. Genetic clustering and phylogenetic methods revealed three distinct groups—one lineage that is highly divergent, and two others that are recently diverged and morphologically similar. A combination of evidence that includes reciprocal monophyly, lack of introgression, and discrete rather than continuous patterns of variation supports the recognition of all three lineages as separate species. These results identify a surprising case of cryptic diversity in which two broadly sympatric species have consistently been lumped in taxonomic treatments. The clarity of our findings is directly related to the dense sampling and high quality genetic data in this study. We argue that there is a critical need for carefully sampled and integrative species delimitation studies to clarify species boundaries even in well-known plant lineages. Studies following the model that we have developed here are likely to identify many more cryptic lineages and will fundamentally improve our understanding of plant speciation and patterns of species richness.
Data from: Sex-biased dispersal obscures species boundaries in integrative species delimitation approaches
Contributors: Eberle, Jonas, Bazzato, Erika, Fabrizi, Silvia, Rossini, Michele, Colomba, Mariastella, Cillo, Davide, Uliana, Marco, Sparacio, Ignazio, Sabatinelli, Guido, Warnock, Rachel
... Accurate delimitation of species is crucial for a stable taxonomy, which provides the foundation for the study of evolutionary biology, ecology and essentially all biological disciplines. Several approaches towards impartial and repeatable taxonomic practices are available but all existing methods have potentially unacceptable shortcomings. In particular, problems can arise when the underlying model assumptions are violated, for instance in the presence of reduced gene flow. This is observed in the context of sex-biased dispersal, which is a common but underappreciated feature in many groups of organisms. Previously, simulations have indicated that sex-biased dispersal may lead to erroneous estimations of the true species numbers. However, this phenomenon has never been examined using empirical data. We evaluate the bias introduced by extreme female philopatry on a range of de novo (GMYC, PTP, ABGD, statistical parsimony, trinomial distribution of triplets model [tr2]) and validation (STACEY, iBPP) approaches to species delimitation in the scarab beetle genus Pachypus. Since female philopatry exhibited in this genus in particular can affect mitochondrial gene flow, we compared the results from analyses of single loci, mitochondrial loci, nuclear loci and combined data, as well as the performance of morphometric data as a secondary data source in a fully integrative Bayesian framework. Large overestimation of species numbers was observed across all analyses of combined and mitochondrial DNA datasets, suggesting specimens from nearly every sampling location as separate species. The use of nuclear data resulted in more reasonable estimations of species boundaries, which were largely supported by morphometrics of linear measurements, while geometric morphometrics of body outlines resulted in stronger splitting. Simulations of population divergence with migration, corresponding to the biology of Pachypus, showed that female philopatry strongly increases reciprocal monophyly of mitochondrial markers and may substantially contribute to over-splitting in species delimitation. Robust results recovered using nuclear DNA and morphological data nevertheless enabled us to reach novel conclusions about species boundaries in Pachypus. Our findings suggest that mitochondrial DNA will be less suited to species delimitation in many cases, in particular in the presence of sex-biased dispersal.
Contributors: Ng, Julienne, Smith, Stacey D.
... Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches, and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short‐term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red‐flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE (Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSE model when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population‐level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.
Contributors: Oaks, Jamie
... A challenge to understanding biological diversification is accounting for community-scale processes that cause multiple, co-distributed lineages to co-speciate. Such processes predict non-independent, temporally clustered divergences across taxa. Approximate-likelihood Bayesian computation (ABC) approaches to inferring such patterns from comparative genetic data are very sensitive to prior assumptions and often biased toward estimating shared divergences. We introduce a full-likelihood Bayesian approach, ecoevolity, which takes full advantage of information in genomic data. By analytically integrating over gene trees, we are able to directly calculate the likelihood of the population history from genomic data, and efficiently sample the model-averaged posterior via Markov chain Monte Carlo algorithms. Using simulations, we find that the new method is much more accurate and precise at estimating the number and timing of divergence events across pairs of populations than existing approximate-likelihood methods. Our full Bayesian approach also requires several orders of magnitude less computational time than existing ABC approaches. We find that despite assuming unlinked characters (e.g., unlinked single-nucleotide polymorphisms), the new method performs better if this assumption is violated in order to retain the constant characters of whole linked loci. In fact, retaining constant characters allows the new method to robustly estimate the correct number of divergence events with high posterior probability in the face of character-acquisition biases, which commonly plague loci assembled from reduced-representation genomic libraries. We apply our method to genomic data from four pairs of insular populations of Gekko lizards from the Philippines that are not expected to have co-diverged. Despite all four pairs diverging very recently, our method strongly supports that they diverged independently, and these results are robust to very disparate prior assumptions.
Data from: A new phylogenetic hypothesis of turtles with implications for the timing and number of evolutionary transitions to marine lifestyles in the group
Contributors: Evers, Serjoscha W., Benson, Roger B. J.
... Evolutionary transitions to marine habitats occurred frequently among Mesozoic reptiles. Only one such clade survives to the present: sea turtles (Chelonioidea). Other marine turtles originated during the Mesozoic, but uncertain affinities of key fossils have obscured the number of transitions to marine life, and the timing of the origin of marine adaptation in chelonioids. Phylogenetic studies support either a highly‐inclusive chelonioid total‐group including fossil marine clades from the Jurassic and Cretaceous (e.g. protostegids, thalassochelydians, sandownids) or a less inclusive chelonioid total‐group excluding those clades. Under this paradigm, these clades belong outside Cryptodira, and represent at least one additional evolutionary transition to marine life in turtles. We present a new phylogenetic hypothesis informed by high resolution computed tomographic data of living and fossil taxa. Besides a well‐supported Chelonioidea, which includes protostegids, we recover a previously unknown clade of stem‐group turtles, Angolachelonia, which includes the Late Jurassic thalassochelydians, and the Cretaceous–Palaeogene sandownids. Accounting for the Triassic Odontochelys, our results indicate three independent evolutionary transitions to marine life in non‐pleurodiran turtles (plus an additional two‐three in pleurodires). Among all independent origins of marine habits, a pelagic ecology only evolved once, among chelonioids. All turtle groups that independently invaded marine habitats in the Jurassic–Cretaceous (chelonioids, angolachelonians, bothremydid pleurodires) survived the Cretaceous–Palaeogene mass extinction event. This highlights extensive survival of marine turtles compared to other marine reptiles. Furthermore, deeply‐nested clades such as chelonioids are found by the middle Early Cretaceous, suggesting a rapid diversification of crown‐group turtles during the Early Cretaceous.