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Brownstein, C.

Publications and source records attributed to Brownstein, C..

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Physiology mediates transcontinental radiations of freshwater fishes

Adaptive radiations are clades that have rapidly accumulated exceptional species richness and ecological diversity. The ability to access sources of ecological opportunity, such as new habitats, is thought to be essential for their success. Transcontinental lineages of exclusively freshwater fishes, such as the 1,700 species of cichlids distributed across Central and South America, Africa, India, and Madagascar, are some of the most celebrated adaptive radiations. Yet, what features facilitated their dispersal across marine barriers and diversification in geologically young freshwater ecosystems remain debated. Here, we show that a common mechanism, saltwater tolerance, provides an explanation for how species-rich transcontinental freshwater fish radiations, including cichlids, killifishes, pupfishes, and livebearers, accessed ecological opportunity and subsequently diversified. Marine salinity tolerance was retained after cichlids, killifishes and their relatives emerged from a rapid radiation during the Cretaceous-Paleogene boundary. The retention of this ancestral physiological trait throughout the last 45 million years of Earth history repeatedly enabled cichlids and other fishes to disperse across marine barriers and radiate in freshwater ecosystems on multiple continents, including geologically young features in Africa and North America that have repeatedly experienced saline conditions over tens of thousands of years of global climate change. These results show how the larger evolutionary context of adaptive radiations can sculpt their responses to ecological opportunity.

evolutionary biology↗

The macroevolutionary impact of an innovation reversal in ray-finned fishes

The evolution of new traits can drive species diversification by facilitating the use of new resources, but environmental change may turn these same adaptations into liabilities.Trait loss is also often associated with the origin of new ecologies, but how losses modulate diversification remains unclear. The swim bladder allows ray-finned fishes to regulate their buoyancy and exploit ecosystems throughout the water column, yet this organ has been lost many times among species-rich lineages. Here, we show that timing and ecological context control the macroevolutionary effects of swim bladder loss. Many lineages of fishes lost the swim bladder over the last 66 million years as they specialized for benthic habitats where buoyancy regulation is unnecessary. Swim bladder loss enabled the descendants of these benthic fishes to diversify in the deep sea where extreme pressure makes its inflation untenable, and in the frigid, oxygen-saturated Southern Ocean, where loss of the oxygen delivery mechanisms required for swim bladder inflation carries little physiological cost. Yet, we detect a selective filter associated with swim bladder loss during extreme global warming 56 to 50 million years ago, when its absence limited the capacity of fishes to escape ecological disruptions on the ocean floor. These contrasting patterns explain how the loss of a complex trait promoted major ecological transitions without increasing overall diversification through deep time. As human activity drives rapid global warming, the evolutionary legacies of swim bladder loss may again shape the fate of marine fish diversity.

evolutionary biology↗

The largest radiations of freshwater fishes initiated at the Cretaceous-Paleogene boundary

Freshwater biodiversity is disproportionally high relative to the limited availability of freshwater habitats. This pattern is exemplified by freshwater fishes. Over 50% of freshwater fish species are concentrated in a single clade, Ostariophysi, including the 5000 species of minnows, carps, and loaches, the 4500 species of catfishes, and the over 2000 species of tetras, pirahnas, and characins. However, the relationships and ages of ostariophysans remain uncertain. We show that the initial diversification of ostariophysans involved only two freshwater invasions and was driven by the strikingly rapid origination of major crown clades, including Neotropical electric fishes, lutefishes, and multiple major living clades of catfishes, carps and minnows, and tetras and characins, within five million years of the Cretaceous-Paleogene mass extinction. This result is congruent with the record of well-preserved body fossils of ostariophysans, but contrasts with the controversial assignment of isolated teeth and bones from the Cretaceous to nested lineages of this set of freshwater fish radiations. Although we confirm that Alepocephaliformes, an obscure marine lineage, is the living sister to Ostariophysi, our results demonstrate that the former clade only recently invaded the deep ocean, a transition that involved the loss of structures essential for enhanced auditory capabilities in ostariophysans and the related herrings and anchovies. These results establish a surprisingly young age for the major lineages of living freshwater fishes.

evolutionary biology↗

Genomic Distortion of Jawed Vertebrate Phylogeny

Reconstructing patterns of evolution requires understanding the interrelationships of species, yet evolutionary relationships that defy resolution and calibration in time are commonplace across the Tree of Life. Here, we investigate the dynamics of temporal and topological uncertainty by generating a phylogeny of jawed vertebrates using 1105 exonic loci sampled for 540 species spanning all major orders and most families of gnathostomes. Across loci and DNA sequence sites, we observe rapid reductions in statistical support for the monophyly of jawed vertebrate clades that originated around the Cretaceous-Paleogene mass extinction. Phylogenetic signal was scrambled to different degrees during rapid successive divergences in multiple unrelated jawed vertebrate lineages that radiated in this interval, including birds, snakes, placental mammals, and acanthomorph fishes. In addition to showing that particular events have modified phylogenetic signal across the same loci in distantly related vertebrate clades, we also demonstrate how rates of genomic evolution affect our ability to infer the timescale of vertebrate evolution. By testing how the inclusion of lineages of ray-finned fishes with very fast and slow rates of molecular evolution changes inferences of the vertebrate evolutionary timescale, we show that the deepest divergences in ray-finned fishes may be impossible to accurately infer using sequence data and calibrations from a limited fossil record. These results hint at the macroevolutionary realities underlying topological and divergence time uncertainty across evolutionary trees.

evolutionary biology↗

Phylogenomics and the origins of sharks

Genomes have the capacity to drastically modify hypotheses about the relationships of species. Despite the growing availability of non-model organism genome sequences, historically contentious portions of Tree of Life remain untested using genomic data. Here, we infer the phylogeny of sharks, skates, rays, and chimaeras using the genomes of 48 species, targeting different genomic marker types. Although phylogenetic relationships of chondrichthyans are relatively consistent across analyses, different molecular markers yield conflicting results about shark monophyly. Exons support the traditional view that sharks are monophyletic, whereas ultraconserved elements and legacy nuclear markers instead suggest that the frilled and cow sharks (Hexanchiformes), which retain the ancestral jaw structure of cartilaginous fishes, is the sister lineage of all other sharks and rays. The resolution of sharks as monophyletic or paraphyletic has little effect on inferences of the timescale of shark evolution or the origins of key traits, such as their ancestral ecology and genome size. We tie the diversification of living cartilaginous fishes to the transformation of marine ecosystems during the middle Mesozoic Era, confirming that living shark diversity is the product of rapid ancient diversification. Consequently, our results suggest that despite uncertainty around whether sharks are monophyletic, consensus can still be reached about major evolutionary events in this iconic vertebrate lineage. Significance StatementLiving sharks, skates, rays, and chimaeras form one of the three principal groups of vertebrates. These iconic animals, which include over 1200 species, are key components of marine ecosystems and have helped us reconstruct the evolution of vertebrate genomes and phenotypes. However, much work on this group has assumed that sharks are a natural group. Here, for the first time, we leverage genome-scale data to test this hypothesis. Surprisingly, we show different genome regions reject or support hypothesis that sharks form a natural group to the exclusion of skates and rays. This throws an unexpected wrench into our understanding of the relationships of some of the oldest living vertebrate clades.

evolutionary biology↗

Reproductive innovation enabled radiation in the deep sea during an ecological crisis

Major ecological transitions are thought to fuel evolutionary radiations, but whether they are contingent on the evolution of certain traits is unclear. We show that the rapid ecological transition of anglerfishes into pelagic habitats during a period of major global warming coincided with the origins of sexual parasitism, in which male anglerfishes temporarily attach or permanently fuse to females to mate. A phylogenomic reconstruction of the evolutionary history of anglerfishes provides a strong inference for the convergent evolution of permanently-fusing deep-sea anglerfishes and their degenerate immune genes. Our results support that sexual parasitism was enabled by the degeneration of adaptive immunity and ancestral sexual size dimorphism. The combination of these traits facilitated the transition of pelagic anglerfishes into novel ecologies available in the deep open oceans after evolving from benthic ancestors. These results show how seemingly unrelated physiological and reproductive traits interact synergistically to drive evolutionary radiation in novel environments.

evolutionary biology↗

Role for the Na+/K+ ATPase α 3 subunit in folding and lamination of the human neocortex

Osmotic equilibrium and membrane potential in animal cells depend on concentration gradients of sodium (Na+) and potassium (K+) ions across the plasma membrane, a function that is catalyzed by the Na,K-ATPase alpha subunit. In vertebrates, four paralogous genes, ATP1A1-4, encode distinct alpha subunit isoforms (a1-a4), three of which (a1, a2, a3) are expressed in the brain, and two (a1, a3) predominantly in neurons. The a3 isoform, encoded by ATP1A3, is critical to neuronal physiology, and a growing spectrum of neurological diseases are associated with ATP1A3 pathogenic variants, with ages of onset ranging from early childhood to adulthood. Here, we describe ATP1A3 variants encoding dysfunctional a3 subunits in children affected by polymicrogyria, a developmental malformation of the cerebral cortex characterized by abnormal folding and laminar organization. To gain cell-biological insights into the spatiotemporal dynamics of prenatal ATP1A3 expression, we established a transcriptional atlas of ATP1A3 expression during cortical development using mRNA in situ hybridization and transcriptomic profiling of ~125,000 individual cells with single-cell RNA sequencing (Drop-Seq) from various areas of the midgestational human neocortex. We find that fetal expression of ATP1A3 is restricted to a subset of excitatory neurons carrying transcriptional signatures of neuronal activity and maturation characteristic of the developing subplate. Furthermore, by performing Drop-Seq on ~52,000 nuclei from four different areas of an infant human neocortex, we show that ATP1A3 expression persists throughout early postnatal development, not only within excitatory neurons across all cortical layers, but also and more predominantly in inhibitory neurons, with specific enrichment in fast-spiking basket cells. In addition, we show that ATP1A3 expression, both in fetal and postnatal neurons, tends to be higher in frontal cortical areas than in occipital areas, in a pattern consistent with the rostro-caudal maturation gradient of the human neocortex. Finally, we discover distinct co-expression patterns linking catalytic subunit isoforms (ATP1A1,2,3) and auxiliary isoforms (ATP1B1,2,3), suggesting the ATPase pump may form non-redundant, cell-type specific -{beta} combinations. Together, the importance of the developmental phenotypes and dynamic expression patterns of ATP1A3 point to a key role for a3 in the development and function of human cortex.

neuroscience↗