J.A. Esselstyn's research while affiliated with Louisiana State University and other places

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Publications (240)


SEGUL: Ultrafast, memory-efficient and mobile-friendly software for manipulating and summarizing phylogenomic datasets
  • Article

April 2024

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62 Reads

Molecular Ecology Resources

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Jacob A Esselstyn

Phylogenetic studies now routinely require manipulating and summarizing thousands of data files. For most of these tasks, currently available software requires considerable computing resources and substantial knowledge of command‐line applications. We develop an ultrafast and memory‐efficient software, SEGUL, that performs common phylogenomic dataset manipulations and calculates statistics summarizing essential data features. Our software is available as standalone command‐line interface (CLI) and graphical user interface (GUI) applications, and as a library for Rust, R and Python, with possible support of other languages. The CLI and library versions run native on Windows, Linux and macOS, including Apple ARM Macs. The GUI version extends support to include mobile iOS, iPadOS and Android operating systems. SEGUL leverages the high performance of the Rust programming language to offer fast execution times and low memory footprints regardless of dataset size and platform choice. The inclusion of a GUI minimizes bioinformatics barriers to phylogenomics while SEGUL's efficiency reduces economic barriers by allowing analysis on inexpensive hardware. Our support for mobile operating systems further enables teaching phylogenomics where access to computing power is limited.

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Three new shrews (Soricidae: Crocidura ) from West Sumatra, Indonesia: elevational and morphological divergence in syntopic sister taxa
  • Article
  • Full-text available

January 2024

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161 Reads

Journal of Mammalogy

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[...]

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Jacob A Esselstyn

We describe 3 new species of shrews (Eulipotyphla, Soricidae, Crocidura) from West Sumatra, Indonesia. Two of these taxa were found above 1,800 m on Mt. Singgalang. The third taxon was found above 1,660 m on Mt. Talamau, 65 km northwest of Mt. Singgalang. We also resurrect Crocidura aequicauda based on 2 specimens from Mts. Tujuh and Kerinci, which lie near the border between West Sumatra and Jambi provinces. Several methodological approaches support our findings: linear cranial morphometrics, landmark-based 2D geometric morphometrics, and molecular phylogenetics using both mtDNA and 6 nuclear exons. A multilocus species-tree analysis places the 3 new species and C. aequicauda in a clade with the Javan endemics C. monticola and C. umbra. Although the 2 taxa from Mt. Singgalang are recovered as sister species, 1 is nearly twice the size of the other, and they are divergent in several other morphological characters, such as tail length, cranium size, and pelage color and texture. Recently diverged yet morphologically disparate sister taxa living syntopically in an isolated habitat “island,” like the montane forests of Mt. Singgalang, is unusual in mammals but documented in other Crocidura on neighboring Java and Borneo; these 2 new taxa represent the first known case of this phenomenon on Sumatra. Our results bring the number of Sumatran Crocidura to 10, 9 of which are endemic to the island. All 3 of the new species appear to be endemic to a single mountain and were not detected in similar surveys of nearby mountains. If this local endemism pattern is common, it would indicate that Sumatra’s mammal diversity may be severely underestimated, largely due to the paucity of small-mammal surveys and museum specimens.

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Specimen collection is essential for modern science

November 2023

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3,847 Reads

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9 Citations

PLOS Biology

PLOS Biology

Natural history museums are vital repositories of specimens, samples and data that inform about the natural world; this Formal Comment revisits a Perspective that advocated for the adoption of compassionate collection practices, querying whether it will ever be possible to completely do away with whole animal specimen collection.


Molecular evolution of male reproduction across species with highly divergent sperm morphology in diverse murine rodents

September 2023

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54 Reads

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1 Citation

Sperm competition can drive the rapid evolution of male reproductive traits, but it remains unclear how variation in sperm competition intensity shapes phenotypic and molecular diversity across clades. Old World mice and rats (subfamily Murinae) comprise one of the most rapid mammalian radiations and exhibit incredible diversity in sperm morphology and production. We sequenced exomes from 36 murine species and combined these data with published sequences to model the evolution of reproductive traits and genes across 78 murine species. We identified several independent shifts towards smaller relative testes mass, a trait reflective of reduced sperm competition. Several features of sperm morphology were associated with relative testes mass, suggesting that mating system evolution likely selects for convergent suites of traits related to sperm competitive ability. Molecular evolutionary rates of spermatogenesis proteins also correlated with relative testes mass, but in an unexpected direction. We predicted that sperm competition would result in rapid divergence among species with large relative testes mass, but instead found that many spermatogenesis genes evolve more rapidly in species with smaller relative testes mass due to relaxed purifying selection. While some reproductive genes showed evidence for pervasive positive selection, relaxed selection played a greater role underlying rapid evolution in small testes species. Our work demonstrates that sexual selection can impose strong purifying selection shaping the evolution of male reproduction.


Figure 1. Al Gardner skinning a bat in 1968 in Perú. Photo credit: John O'Neill.
Figure 2. Al Gardner holding a Red-throated Caracara in 1968 in Perú. Photo credit: John O'Neill.
Figure 3. Al Gardner thinking deeply about neotropical mammals in Balta, Perú. Photo credit: Jim Patton.
Editorial. Special Issue in Honor of Dr. Alfred L. Gardner

January 2023

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420 Reads

Therya

It is a great pleasure to introduce this special feature honoring Dr. Alfred Lunt Gardner. Al’s many contributions to mammalogy span seven decades, two continents, and practically the entire tree of mammals. It is impossible to imagine what mammalogy in the Americas would look like without him. His academic contributions are as significant as his imposing stature. Al was born in Salem, Massachusetts in 1937 and spent his early childhood there. His first interests in natural history were sparked by his 3rd-grade teacher, an amateur ornithologist who kept a cabinet of specimens in her classroom (Gardner 2005). In 1947, the Gardner family relocated to a farm in North Andover, Massachusetts, where, according to Al, he “practically lived in the woods fishing, hunting, and trapping” (pg. 277, Gardner 2005). In his adolescent years, Al would spend considerable time in the outdoors, honing his trapping and skinning skills. By his freshman year of high school, he was selling furs and evading game wardens (Gardner 2005). In 1953, his family moved to Tucson, Arizona, where Al found a trove of new habitats and wildlife to explore. By 1955, Al graduated high school, signed up for the Army Reserves, and enrolled at the University of Arizona, where his mammalogical interests would be further stimulated by E. Lendell Cockrum and his graduate students.


Map of northern Borneo showing the type locality of Suncus ater (Mount Kinabalu) and recently surveyed sites in Sarawak (Mounts Mulu and Murud).
Maximum-likelihood crocidurine mitochondrial gene tree inferred in IQTree. Bootstrap values are given at the nodes. The holotype of ater (MCZ36574) forms a clade with the specimens recently collected in Sarawak. The outgroup branch to Myosorex kihaulei has been truncated.
Phylogenetic hypotheses from UCE data. The tree topologies are very similar between the two methods. A phylogenetic tree inferred using 3,757 concatenated UCE loci (2,175,243 base pairs) in IQTree. Bootstrap supports are provided at the nodes. The branch leading to outgroup Myosorex kihaulei has been truncated for display B species tree inferred using ASTRAL. Nodal supports are given in local posterior probabilities. ASTRAL tree is presented as ultrametric with uninformative branch lengths.
The holotype of Palawanosorex ater largely matches the external and cranial measurements of P. ater specimens captured in Sarawak, not P. muscorum. Each panel represents a measurement, and the y-axis represents the measurement length in mm. Each species is represented by a different shape. The upper and lower bounds of the point intervals represent the maximum and minimum values for each measurement for each species. Measurements are limited to those reported in the description of Suncus ater (Medway 1965). Palawanosorex ater measurements are taken from six specimens collected in Sarawak, Malaysia. Palawanosorex muscorum measurements are taken from Hutterer et al. (2018: tables 1, 2). LSUMZ 40695 has a cropped tail and was removed from the total length and tail length measurements.
A dorsal and ventral views of the cranium of LSUMZ 40697, Palawanosorex ater, collected on Mount Murud, Sarawak, Malaysia. Photo by Heru Handika B dorsal and ventral views of the holotype of P. ater, MCZ 36574, collected on Mt. Kinabalu, Sabah, Malaysia. Photo by Museum of Comparative Zoology, Harvard University, President and Fellows of Harvard College.
Molecular data from the holotype of the enigmatic Bornean Black Shrew, Suncus ater Medway, 1965 (Soricidae, Crocidurinae), place it in the genus Palawanosorex

December 2022

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183 Reads

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2 Citations

Although Borneo has received more attention from biologists than most other islands in the Malay Archipelago, many questions regarding the systematic relationships of Bornean mammals remain. Using next-generation sequencing technology, we obtained mitochondrial DNA sequences from the holotype of Suncus ater , the only known specimen of this shrew. Several shrews collected recently in Sarawak are closely aligned, both morphologically and mitochondrially, with the holotype of S. ater . Phylogenetic analyses of mitochondrial sequences indicate that the S. ater holotype and new Sarawak specimens do not belong to the genus Suncus , but instead are most closely related to Palawanosorex muscorum . Until now Palawanosorex has been known only from the neighboring Philippine island of Palawan. Additional sequences from nuclear ultra-conserved elements from the new Sarawak specimens strongly support a sister relationship to P. muscorum . We therefore transfer ater to Palawanosorex . The new specimens demonstrate that P. ater is more widespread in northern Borneo than previously recorded. Continued sampling of Bornean mammal diversity and reexamination of type material are critical in understanding the evolutionary history of the biologically rich Malay Archipelago.


Mycoplasmataceae dominate microbial community differences between gut regions in mammals with a simple gut architecture

November 2022

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24 Reads

Journal of Mammalogy

Faunivorous mammals with simple guts are thought to rely primarily on endogenously produced enzymes to digest food, in part because they lack fermentation chambers for facilitating mutualistic interactions with microbes. However, variation in microbial community composition along the length of the gastrointestinal tract has yet to be assessed in faunivorous species with simple guts. We tested for differences in bacterial taxon abundances and community compositions between the small intestines and colons of 26 individuals representing four species of shrew in the genus Crocidura. We sampled these hosts from a single locality on Sulawesi Island, Indonesia, to control for potential geographic and temporal variation. Bacterial community composition differed significantly between the two gut regions and members of the family Mycoplasmataceae contributed substantially to these differences. Three operational taxonomic units (OTUs) of an unclassified genus in this family were more abundant in the small intestine, whereas 1 OTU of genus Ureaplasma was more abundant in the colon. Species of Ureaplasma encode an enzyme that degrades urea, a metabolic byproduct of protein catabolism. Additionally, a Hafnia–Obesumbacterium OTU, a genus known to produce chitinase in bat gastrointestinal tracts, was also more abundant in the colon compared to the small intestine. The presence of putative chitinase- and urease-producing bacteria in shrew guts suggests mutualisms with microorganisms play a role in facilitating the protein-rich, faunivorous diets of simple gut mammals.


Figure 1. Map of southern Mexico showing the geographic ranges of the Peromyscus mexicanus subspecies, with samples analyzed in this work (yellow circles) and type localities of each subspecies (red diamonds) shown. Map modified from Pardiñas et al. (2017), Pérez-Consuegra and Vázquez-Domínguez (2017), and Trujano-Álvarez and Álvarez-Castañeda (2010).
Figure 2. Majority rule consensus tree obtained from Bayesian analysis of cytochrome b sequences, in the P. mexicanus species group. Support values are shown as posterior probabilities followed by bootstrap values from a maximum likelihood analysis. Support values < 0.8/80 are not shown. Numbers I to IV correspond to the 4 main clades detected in this species group; nomenclature of clades according to Pérez-Consuegra and Vázquez-Domínguez (2017). Note that P. m. teapensis, P. m. tehuantepecus, and P. m. totontepecus (in the orange box), are sister to P. gymnotis, and not to P. m. mexicanus. Label tips show country (CR = Costa Rica, ES = El Salvador, GT = Guatemala, HO = Honduras, MX = Mexico, NI = Nicaragua), states/provinces/departments (cg = Cartago, sj = San José; ct = Chalatenango; av = Alta Verapaz, ch = Chimaltenango, ep = El Progreso, es = Escuintla, gt = Guatemala, hu = Huehuetenango, iz = Izabal, ju = Jutiapa, qe = Quetzaltenango, qc = Quiche, sr = Santa Rosa, su = Suchitepequez; ol = Olancho, le = Lempira; cs = Chiapas, gr = Guerrero, hi = Hidalgo, oa = Oaxaca, ta = Tabasco, ve = Veracruz; et = Estelí), and catalog number of each analyzed specimen.
Figure 3. Heat map showing genetic distances in the P. mexicanus species group. Interspecific and intraspecific comparison are shown above and below the black line, respectively. Sample-specific labels are shown on both axes, showing the country (CR = Costa Rica, ES = El Salvador, GT = Guatemala, HO = Honduras, MX = Mexico, NI = Nicaragua), states/provinces/departments (cg = Cartago, sj = San José; ct = Chalatenango; av = Alta Verapaz, ch = Chimaltenango, ep = El Progreso, es = Escuintla, gt = Guatemala, hu = Huehuetenango, iz = Izabal, ju = Jutiapa, qe = Quetzaltenango, qc = Quiche, sr = Santa Rosa, su = Suchitepequez; ol = Olancho, le = Lempira; cs = Chiapas, gr = Guerrero, hi = Hidalgo, oa = Oaxaca, ta = Tabasco, ve = Veracruz; et = Estelí), and catalog number of each analyzed specimen. Nomenclature of clades according to Pérez-Consuegra and Vázquez-Domínguez (2017).
Paraphyletic relationships revealed by mitochondrial DNA in the Peromyscus mexicanus species group (Rodentia: Cricetidae)

August 2022

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172 Reads

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4 Citations

REVISTA MEXICANA DE BIODIVERSIDAD

Although deer mice (Peromyscus spp.) are among the most studied small mammals, their species diversity and phylogenetic relationships remain unclear. The lack of taxonomic clarity is mainly due to a conservative morphology and because some taxa are rare, have restricted distributions, or are poorly sampled. One taxon, P. mexicanus, includes southern Mexican subspecies that have not had their systematic placement tested with genetic data. We analyzed the phylogenetic relationships and genetic structure of P. mexicanus populations using sequences of the mitochondrial gene cytochrome b. We inferred that P. mexicanus is paraphyletic, with P. m. teapensis, P. m. tehuantepecus, andP. m. totontepecus more closely related to P. gymnotis than to P. m. mexicanus. This highly divergent clade ranges from northeastern Oaxaca to northern Chiapas, including southern Veracruz, and southern Tabasco. In light of this group’s mitochondrial distinctiveness, cohesive geographic range, and previously reported molecular, biochemical, and morphological differences, we recommend it be treated as P. totontepecus. Our findings demonstrate the need for an improved understanding of the diversity and evolutionary history of these common and abundant members of North American small mammal communities.


Summary of findings of literature search identifying all mammals screened for Pneumocystis. Number of mammal species, genera, and orders sampled for Pneumocystis screening. Percentages of total mammal diversity are shown as well as the proportion of species from which Pneumocystis genetic sequences are available.
Number of species screened per sampled mammal order. The 12 unsampled mammal orders are not listed.
Predicting Species Boundaries and Assessing Undescribed Diversity in Pneumocystis, an Obligate Lung Symbiont

July 2022

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72 Reads

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2 Citations

Journal of Fungi

Far more biodiversity exists in Fungi than has been described, or could be described in several lifetimes, given current rates of species discovery. Although this problem is widespread taxonomically, our knowledge of animal-associated fungi is especially lacking. Fungi in the genus Pneumocystis are obligate inhabitants of mammal lungs, and they have been detected in a phylogenetically diverse array of species representing many major mammal lineages. The hypothesis that Pneumocystis cospeciate with their mammalian hosts suggests that thousands of Pneumocystis species may exist, potentially equal to the number of mammal species. However, only six species have been described, and the true correspondence of Pneumocystis diversity to host species boundaries is unclear. Here, we use molecular species delimitation to estimate the boundaries of Pneumocystis species sampled from 55 mammal species representing eight orders. Our results suggest that Pneumocystis species often colonize several closely related mammals, especially those in the same genus. Using the newly estimated ratio of fungal to host diversity, we estimate ≈4600 to 6250 Pneumocystis species inhabit the 6495 currently recognized extant mammal species. Additionally, we review the literature and find that only 240 (~3.7%) mammal species have been screened for Pneumocystis, and many detected Pneumocystis lineages are not represented by any genetic data. Although crude, our findings challenge the dominant perspective of strict specificity of Pneumocystis to their mammal hosts and highlight an abundance of undescribed diversity.


Trait-specific patterns of community ecospace occupancy in an insular mammal radiation

July 2022

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21 Reads

Communities that occupy similar environments but vary in the richness of closely related species can illuminate how functional variation and species richness interact to fill ecological space in the absence of abiotic filtering, though this has yet to be explored on an oceanic island where the processes of community assembly may differ from continental settings. In discrete montane communities on the island of Sulawesi, local murine rodent (rats and mice) richness ranges from 7 to 23 species. We measured 17 morphological, ecological, and isotopic traits, both individually and grouped into 5 multivariate traits in 40 species, to test for the expansion or packing of functional space among nine murine communities. We employed a novel probabilistic approach for integrating intraspecific and community-level trait variance into functional richness. Trait-specific and phylogenetic diversity patterns indicate dynamic community assembly due to variable niche expansion and packing on multiple niche axes. Locomotion and covarying traits such as tail length emerged as a fundamental axis of ecological variation, expanding functional space and enabling the niche packing of other traits such as diet and body size. Though trait divergence often explains functional diversity in island communities, we found that phylogenetic diversity facilitates functional space expansion in some conserved traits such as cranial shape, while more labile traits are overdispersed both within and between island clades, suggesting a role of niche complementarity. Our results evoke interspecific interactions, differences in trait lability, and the independent evolutionary trajectories of each of Sulawesi’s 6 murine clades as central to generating the exceptional functional diversity and species richness in this exceptional, insular radiation. Bahasa Indonesia Abstract translation to be provided in subsequent version.


Citations (52)


... Finally, these records, housed in long-term public museums, highlight the importance of zoological collections through time and reinforce that they are timeless treasures (Koch et al. 2019), particularly in this time of rapid environmental changes, contributing to the global development of science (Nachman et al. 2023). ...

Reference:

First record of Plectrohyla guatemalensis Brocchi, 1877 (Anura, Hylidae) from Nicaragua
Specimen collection is essential for modern science
PLOS Biology

PLOS Biology

... Diversification of neotomines in general and Peromyscus in particular occurred during the late Miocene and the Pliocene [30]. At present, and based on recent revisions using molecular and morphometric analysis, the P. mexicanus species group is considered a monophyletic group of Pleistocene origin [31], which currently includes 12 mountain species, P. nudipes, P. tropicalis, P. mexicanus, P. gymnotis, P. zarhynchus, P. gardneri, P. salvadorensis, P. nicaraguae, P. guatemalensis, P. grandis, P. carolpattonae, and P. bakeri [17,20,[32][33][34][35], distributed at lowlands and highlands across Guatemala-Chiapas and Central America mountains. ...

Paraphyletic relationships revealed by mitochondrial DNA in the Peromyscus mexicanus species group (Rodentia: Cricetidae)

REVISTA MEXICANA DE BIODIVERSIDAD

... As part of this latter step, we created two data matrices of UCE loci where each locus had 75% (1) and 100% (2) of the taxa represented in each alignment, respectively. Summary statistics were computed using SEGUL 0.16.3 (Handika and Esselstyn, 2022). ...

SEGUL: An ultrafast, memory-efficient alignment manipulation and summary tool for phylogenomics
  • Citing Preprint
  • May 2022

... More recently, using molecular data Durish et al. (2004), Fernández (2011), andHernández-Canchola et al. (2022) provided evidence for the monophyly of the difficilis-nasutus-griseus group, but within-group relationships remained unresolved. Durish et al. (2004) found two lineages, one from south-central Mexico and another including one sample from the Sierra Madre Occidental (SMOc) and two samples from the USA. ...

Mitochondrial DNA and other lines of evidence clarify species diversity in the Peromyscus truei species group (Cricetidae: Neotominae)

Mammalia

... The ongoing effort to document global biodiversity has revealed that the number of living mammal species has been greatly underestimated, particularly in diverse tropical regions (Reeder et al. 2007;Heaney et al. 2016;Esselstyn et al. 2021;Parsons et al. 2022). Intense anthropogenic pressures exerted across the global tropics today add urgency to the need to accurately document biodiversity. ...

Fourteen New, Endemic Species of Shrew (Genus Crocidura) from Sulawesi Reveal a Spectacular Island Radiation
  • Citing Article
  • December 2021

Bulletin of the American Museum of Natural History

... ferrunginea) to woodrats in southern Mexico and portions of northern Central America; resulting in the placement of N. isthmica into synonymy with N. ferrunginea. In addition, Hernández-Canchola et al. (2021) subsumed two additional subspecies of N. mexicana (tropicalis and solitaria) into N. ferrunginea further solidifying the status of that taxon. Fourth, Fernández (2014) reevaluated the status of N. nelsoni and suggested it was no more than a subspecies of N. leucodon. ...

Mitochondrial DNA indicates paraphyletic relationships of disjunct populations in the Neotoma mexicana species group

... This ecological trait is possibly related to the fact that the Isthmus of Tehuantepec does not represent a severe geographic barrier to V. villai, which has some populations located east of the isthmus. The same pattern is observed in some lowland rodents such as species of Neotoma and Peromyscus (Hernández-Canchola et al. 2021. ...

Mitochondrial DNA indicate paraphyletic relationships and resolve disjunct distributions in the Neotoma mexicana species group

Therya

... Another approach exploits the information on extinction provided by the fossil record to inform phylogenetic diversification analyses, by first independently estimating the temporal dynamics of extinction from fossil data (Upham et al. 2021, Quintero et al. 2024). These extinction curves are then used to perform phylogenetic inference on speciation. ...

Molecules and fossils tell distinct yet complementary stories of mammal diversification

Current Biology

... Sperm competition often leads to the rapid evolution of male reproductive traits (1)(2)(3)(4)(5), which can drive both extreme phenotypic divergence within populations (1) and the evolution of reproductive barriers between nascent species (6). Rapid evolution of reproduction also occurs at the molecular level, with reproductive genes tending to show rapid protein sequence evolution (7)(8)(9)(10)(11). Rapid protein-coding divergence is often attributed to pervasive positive selection (7,8), but other processes such as relaxed purifying selection may be common for tissue-specific male reproductive genes (12)(13)(14)(15)(16). ...

Molecular Evolution of Ecological Specialisation: Genomic Insights from the Diversification of Murine Rodents

Genome Biology and Evolution

... We found that diadromous lineages show convergence in multivariate trait space (Table 3) and on some, but not all univariate locomotor traits (Figure 4). The locomotor performance of fishes is a primary axis of morphological (Dornburg et al. 2011;Astudillo-Clavijo et al. 2015;Nations et al. 2020;Friedman et al. 2021) and physiological (Lee et al. 2003;Dalziel et al. 2012; This is the author's accepted manuscript without copyediting, formatting, or final corrections. It will be published in its final form in an upcoming issue of The American Naturalist, published by Bloom 2020) and are consistent with biomechanical theory for prolonged swimming performaces (i.e. ...

Locomotory mode transitions alter phenotypic evolution and lineage diversification in an ecologically rich clade of mammals
  • Citing Article
  • December 2020

Evolution