Cave-adapted evolution in the North American amblyopsid fishes inferred using phylogenomics and geometric morphometrics

© 2020 The Authors. Evolution © 2020 The Society for the Study of Evolution. Cave adaptation has evolved repeatedly across the Tree of Life, famously leading to pigmentation and eye degeneration and loss, yet its macroevolutionary implications remain poorly understood. We use the North American amblyopsid fishes, a family spanning a wide degree of cave adaptation, to examine the impact of cave specialization on the modes and tempo of evolution. We reconstruct evolutionary relationships using ultraconserved element loci, estimate the ancestral histories of eye-state, and examine the impact of cave adaptation on body shape evolution. Our phylogenomic analyses provide a well-supported hypothesis for amblyopsid evolutionary relationships. The obligate blind cavefishes form a clade and the cave-facultative eyed spring cavefishes are nested within the obligate cavefishes. Using ancestral state reconstruction, we find support for at least two independent subterranean colonization events within the Amblyopsidae. Eyed and blind fishes have different body shapes, but not different rates of body shape evolution. North American amblyopsids highlight the complex nature of cave-adaptive evolution and the necessity to include multiple lines of evidence to uncover the underlying processes involved in the loss of complex traits

Living in the Past: Phylogeography and Population Histories of Indo-Pacific Wrasses (Genus Halichoeres) in Shallow Lagoons versus Outer Reef Slopes

Sea level fluctuations during glacial cycles affect the distribution of shallow marine biota, exposing the continental shelf on a global scale, and displacing coral reef habitat to steep slopes on oceanic islands. In these circumstances we expect that species inhabiting lagoons should show shallow genetic architecture relative to species inhabiting more stable outer reefs. Here we test this expectation on an ocean-basin scale with four wrasses (genus Halichoeres): H. claudia (N = 194, with ocean-wide distribution) and H. ornatissimus (N = 346, a Hawaiian endemic) inhabit seaward reef slopes, whereas H. trimaculatus (N = 239) and H. margaritaceus (N = 118) inhabit lagoons and shallow habitats throughout the Pacific. Two mitochondrial markers (cytochrome oxidase I and control region) were sequenced to resolve population structure and history of each species. Haplotype and nucleotide diversity were similar among all four species. The outer reef species showed significantly less population structure, consistent with longer pelagic larval durations. Mismatch distributions and significant negative Fu’s F values indicate Pleistocene population expansion for all species, and (contrary to expectations) shallower histories in the outer slope species. We conclude that lagoonal wrasses may persist through glacial habitat disruptions, but are restricted to refugia during lower sea level stands. In contrast, outer reef slope species have homogeneous and well-connected populations through their entire ranges regardless of sea level fluctuations. These findings contradict the hypothesis that shallow species are less genetically diverse as a consequence of glacial cycles

The genetic basis and evolution of red blood cell sickling in deer

Crescent-shaped red blood cells, the hallmark of sickle-cell disease, present a striking departure from the biconcave disc shape normally found in mammals. Characterized by increased mechanical fragility, sickled cells promote haemolytic anaemia and vaso-occlusions and contribute directly to disease in humans. Remarkably, a similar sickle-shaped morphology has been observed in erythrocytes from several deer species, without obvious pathological consequences. The genetic basis of erythrocyte sickling in deer, however, remains unknown. Here, we determine the sequences of human β-globin orthologues in 15 deer species and use protein structural modelling to identify a sickling mechanism distinct from the human disease, coordinated by a derived valine (E22V) that is unique to sickling deer. Evidence for long-term maintenance of a trans-species sickling/non-sickling polymorphism suggests that sickling in deer is adaptive. Our results have implications for understanding the ecological regimes and molecular architectures that have promoted convergent evolution of sickling erythrocytes across vertebrates

Summary statistics for slope species.

<p>Summary statistics for slope species based on sample location. Control region values are in bold, and follow CO1 values. Number of individuals (N), number of haplotypes (N_h), haplotype diversity (h), nucleotide diversity (π), and Fu’s F statistic are given for each location sampled. FFS  =  French Frigate Shoals.</p

Haplotype diversities for each of four <i>Halichoeres</i> species.

<p>Haplotype diversities for each of four <i>Halichoeres</i> species with error bars. CO1 (dark grey) indicates diversities for the cytochrome oxidase subunit 1 fragment, CR (light grey) indicates diversities for the control region fragment.</p

Control region haplotype networks for all species.

<p>Minimum spanning networks showing CR haplotype relationships for A) <i>Halichoeres claudia</i>, B) <i>H. trimaculatus</i>, C) <i>H. margaritaceus</i>. <i>H. ornatissimus</i> is not shown. Perpendicular bars and open squares represent single mutational steps between haplotypes, while closed squares represent 10 mutational steps.</p

Simulated mismatch distributions for each species and molecular marker.

<p>Observed mismatch distributions are represented by the bar graphs, while the curve represents the simulated distribution. P-values are reported for each marker. A) <i>Halichoeres claudia</i>, B) <i>H. ornatissimus</i>, C) <i>H. trimaculatus</i>, D) <i>H. margaritaceus</i>.</p

Population pairwise Φ_ST values for <i>H. margaritaceus.</i>

<p>Pairwise Φ_ST values for <i>H. margaritaceus</i> based on sampling location. Values for CO1 are given below the diagonal, while CR values are reported above.</p>*<p>significant at <i>P</i> = 0.05.</p