Evolution in Sinocyclocheilus cavefish is marked by rate shifts, reversals, and origin of novel traits

Abstract

Background Natural model systems are indispensable for exploring adaptations in response to environmental pressures. Sinocyclocheilus of China, the most diverse cavefish clade in the world (75 species), provide unique opportunities to understand recurrent evolution of stereotypic traits (such as eye loss and sensory expansion) in the context of a deep and diverse phylogenetic group. However, they remain poorly understood in terms of their morphological evolution. Therefore, we explore key patterns of morphological evolution, habitat utilization and geographic distribution in these fishes. Results We constructed phylogenies and categorized 49 species based on eye-related condition (Blind, Micro-eyed, and Normal-eyed), habitat types (Troglobitic—cave-restricted; Troglophilic—cave-associated; Surface—outside caves) and existence of horns. Geometric-morphometric analyses show Normal-eyed morphs with fusiform shapes segregating from Blind/Micro-eyed deeper bodied morphs along the first principal-component axis; second axis accounts for shape complexity related to horns. The body shapes showed a significant association with eye-related condition and horn, but not habitat types. Ancestral reconstructions suggest at least three independent origins of Blind morphs, each with different levels of modification in relation to their ancestral Normal-eyed morphs; Sinocyclocheilus are also pre-adapted for cave dwelling. Our geophylogeny shows an east-to-west diversification spanning Pliocene and Pleistocene, with early-diversifying Troglobitic species dominating subterranean habitats of karstic plains whereas predominantly Surface forms inhabit hills to the west. Evolutionary rates analyses suggest that lineages leading to Blind morphs were characterized by significant rate shifts, such as a slowdown in body size evolution and a 5–20 fold increase in rate of eye regression, possibly explained by limited resource availability. Body size and eye size have undergone reversals, but not horns, a trait entailing considerable time to form. Conclusions Sinocyclocheilus occupied cave habitats in response to drying associated with aridification of China during late Miocene and the Pliocene. The prominent cave-adaptations (eye-regression, horn-evolution) occur in clades associated with the extensive subterranean cave system in Guangxi and Guizhou provinces. Integration of morphology, phylogeny, rate analyses, molecular-dating and distribution show not only several remarkable patterns of evolution, but also interesting exceptions to these patterns signifying the diversification of Sinocyclocheilus as an invaluable model system to explore evolutionary novelty.

Whole-Genome Sequencing of Sinocyclocheilus maitianheensis Reveals Phylogenetic Evolution and Immunological Variances in Various Sinocyclocheilus Fishes

“…A progressive evolutionary relationship in the five Sinocyclocheilus species revealed a new phylogeny based on both genome and transcriptome data (Figure 1C). This topology is consistent with the phylogenetic tree based on genomes (Yang et al, 2016) and mitochondrial genes (Zhang and Wang, 2018), but it is different from a previous report of a division into two branches, in which S. maitianheensis, S. anophthalmus, and S. anophthalmus are located in one branch, whereas S. anshuiensis and S. rhinocerous are located in another branch (Mao et al, 2021) based on the morphological trait of eyes. Therefore, our latest topology provides novel insights into detailed phylogeny for the five Sinocyclocheilus species at a genome level.…”

Adapting to novel environments together: evolutionary and ecological correlates of the bacterial microbiome of the world’s largest cavefish diversification

“…We estimated genetic distance matrices for cytb and ND4 genes using Mega X software for 24 species of Sinocyclocheilus. Also, some data was derived from a published paper from our laboratory (Mao et al, 2021). Phylogenetic distance matrix was used to perform Mantel tests (R packagevegan 2.5.7) with the host microbial similarity distance matrix.…”

“…The gastrointestinal tract of an animal is occupied by a microbiome, a staggering diversity of microbial colonies that are in a symbiotic association with the host (Hooper, 2015). These commensal gut-bacterial relationships influence many vital aspects of the host, such as immune function, nutrient absorption, development, and behavior (Mazmanian et al, 2005;Nicholson et al, 2005;Mcfall-Ngai et al, 2013). Hence, the gut microbiome is considered an extension of the host genome, and these microbes are thought to have served as a "bridge" between the host and the external environment during evolution (Shapira and Michael., 2016).…”

“…Although large troglomorphic diversifications are rare, one such radiation exists in a group of freshwater fishes in China. Sinocyclocheilus (Cyprinidae, Barbinae), the largest cavefish diversification in the world, represents an emerging model system for evolutionary novelty (Mao et al, 2021), provides an invaluable opportunity for examining the associations between host evolutionary history, environment and gut-microbial community diversity. With almost 75 extant species, Sinocyclocheilus is a monophyletic group of cyprinid cavefishes endemic to the expansive southwestern karstic region of China, the largest limestone area in the world, with an area ca.…”

“…They are classified into three major habitat types as Troglobitic (exclusively cave species), Troglophilic (associated with caves), and Surface (non-cave dependent species). These habitat types are correlated with their morphological adaptation, especially of their eye condition: Normal-Eyed (Surface), Micro-eyed (Troglophilic) and Blind (Troglobitic) (Mao et al, 2021).…”