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Harrington, R. C.

Publications and source records attributed to Harrington, R. C..

6 recordsLinked to original sources

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↗

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↗

Lacustrine speciation associated with chromosomal inversion in a lineage of riverine fishes

Geographic isolation is the primary driver of speciation in many vertebrate lineages. This trend is exemplified by North American darters, a clade of freshwater fishes where nearly all sister species pairs are allopatric and separated by millions of years of divergence. One of the only exceptions is the Lake Waccamaw endemic Etheostoma perlongum and its riverine sister species E. maculaticeps, which have no physical barriers to gene flow. Here we show that lacustrine speciation of E. perlongum is characterized by morphological and ecological divergence likely facilitated by a large chromosomal inversion. While Etheostoma perlongum is phylogenetically nested within the geographically widespread E. maculaticeps, there is a sharp genetic and morphological break coinciding with the lake-river boundary in the Waccamaw River system. Despite recent divergence, an active hybrid zone, and ongoing gene flow, analyses using a de novo reference genome reveal a 9 Mb chromosomal inversion with elevated divergence between E. perlongum and E. maculaticeps. This region exhibits striking synteny with known inversion supergenes in two distantly related fish lineages, suggesting deep evolutionary convergence of genomic architecture. Our results illustrate that rapid, ecological speciation with gene flow is possible even in lineages where geographic isolation is the dominant mechanism of speciation.

evolutionary biology↗

Widespread sympatry in a species-rich clade of marine fishes (Carangoidei)

The patterns of speciation in marine fishes are largely unknown, in part due to the deficiency of species-level phylogenies and information on species distributions, and partly due to conflicting relationships between species dispersal, range size, and patterns of co- occurrence. Most research on global patterns of marine fish speciation has focused on coral reef or pelagic species. Carangoidei is a clade of marine fishes including the trevallies, remoras, and dolphinfishes that utilize both coral reef and pelagic environments, spanning the ecologies of coral reef obligate and open-ocean species. We used sequence capture of 1314 ultraconserved elements (UCEs) from 154 taxa to generate a phylogeny of Carangoidei and its parent clade, Carangiformes. Age-range correlation analyses of the geographic distributions and divergence times of sister species pairs reveal widespread sympatry, with 73% of sister species pairs exhibiting a sympatric geographic distribution, regardless of node age, and most species pairs co-existing across large portions of their ranges. We also observe greater disparity in body size and water column depth utilization between sympatric than allopatric sister species. These and other ecological or behavioral attributes likely facilitate sympatry among the most closely related carangoid species, which exhibit sympatry at a larger taxonomic scale than has previously been described in marine fishes.

evolutionary biology↗

Prolonged morphological expansion of spiny-rayed fishes following the end-Cretaceous

Spiny-rayed fishes (Acanthomorpha) dominate modern marine habitats and comprise more than a quarter of all living vertebrate species1-3. It is believed that this dominance resulted from explosive lineage and phenotypic diversification coincident with the Cretaceous-Paleogene (K-Pg) mass-extinction event4. It remains unclear, however, if living acanthomorph diversity is the result of a punctuated burst or gradual accumulation of diversity following the K-Pg. We assess these hypotheses with a time-calibrated phylogeny inferred using ultraconserved elements from a sampling of species that represent over 91% of all acanthomorph families, as well as an extensive body shape dataset of extant species. Our results indicate that several million years after the end-Cretaceous, acanthomorphs underwent a prolonged and significant expansion of morphological disparity primarily driven by changes in body elongation, and that acanthomorph lineages containing the bulk of the living species diversity originated throughout the Cenozoic. These acanthomorph lineages radiated into distinct regions of morphospace and retained their iconic phenotypes, including a large group of laterally compressed reef fishes, fast-swimming open-ocean predators, bottom-dwelling flatfishes, seahorses, and pufferfishes. The evolutionary success of spiny-rayed fishes is the culmination of a post K-Pg adaptive radiation in which rates of lineage diversification were decoupled from periods of high phenotypic disparity.

evolutionary biology↗