Niemiller, M. | bioRxiv Science

bioRxiv2024

Ancient climate changes and relaxed selection shape cave colonisation in North American cavefishes

Extreme environments serve as natural laboratories for studying evolutionary processes, with caves offering replicated instances of independent colonisations. The timing, mode, and genetic underpinnings underlying cave-obligate organismal evolution remains enigmatic. We integrate phylogenomics, fossils, paleoclimatic modeling, and newly sequenced genomes to elucidate the evolutionary history and adaptive processes of cave colonisation in the study group, the North American Amblyopsidae fishes. Amblyopsid fishes present a unique system for investigating cave evolution, encompassing surface, facultative cave-dwelling, and cave-obligate (troglomorphic) species. Using 1,105 exon markers and total-evidence dating, we reconstructed a robust phylogeny that supports the nested position of eyed, facultative cave-dwelling species within blind cavefishes. We identified three independent cave colonisations, dated to the Early Miocene (18.5 Mya), Late Miocene (10.0 Mya), and Pliocene (3.0 Mya). Evolutionary model testing supported a climate-relict hypothesis, suggesting that global cooling trends since the Early-Middle Eocene may have influenced cave colonisation. Comparative genomic analyses of 487 candidate genes revealed both relaxed and intensified selection on troglomorphy-related loci. We found more loci under relaxed selection, supporting neutral mutation as a significant mechanism in cave-obligate evolution. Our findings provide empirical support for climate-driven cave colonisation and offer insights into the complex interplay of selective pressures in extreme environments.

evolutionary biology↗

bioRxiv2019

Variation in cephalic neuromasts surface and cave-dwelling fishes of the family Amblyopsidae (Teleostei: Percopsiformes)

Cave adaptation has led to unique sensory specializations to compensate for the lack of visual cues in aphotic subterranean habitats. As the role of vision is reduced or disappears, other sensory modalities become hypertrophied allowing cave-adapted organisms to successfully detect and interact their surrounding environment. The array of aquatic subterranean habitats, from fast-flowing streams and waterfalls, to quiet phreatic pools, presents a diverse palette to examine what possible sensory solutions have evolved against a backdrop of complete darkness. Mechanosensation is enhanced in many subterranean animals to such an extent that a longer appendage is recognized as a prominent troglomorphic adaptation in many metazoans. Fishes, however, not only interact with the environment using their fins, but also with specialized sensory organs to detect hydrodynamic events. We hypothesize that subterranean adaptation drives the hypertrophy of the mechanosensory lateral line, but that other environmental forces dictate the specific neuromast phenotype. To this end, we studied differences in the cephalic lateral line of the fishes in the North American family Amblyopsidae, which includes surface, cave-facultative, and cave-obligate species. None of the taxa we examined possessed canal neuromasts on the head. Primarily surface-dwelling species, Chologaster cornuta and Forbesichthys agassizii, possessed receded neuromasts throughout most of the head, with a few on papillae located in front of the nostrils and on ventral grooves on each side of the mouth. The cavefishes Amyblopsis spelaea and Typhlichthys subterraneous possessed papillate superficial neuromasts all over the head. We speculate that the change from the surface to the cave environment has led to papillate neuromasts in this group, which are likely shaped to detect the hydrodynamic characteristics of the boundary layer created by the swimming fish. Moving sensory organs from the surface of the body out into the boundary layer could increase sensitivity to high frequency stimuli created by prey, predators, and conspecifics.

zoology↗