 |
| Sinocyclocheilus spp. in Mao, Liu, Meegaskumbura, ... et al., 2021. |
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.
Keywords: Phylomorphospace, Evolutionary convergence, Blind fish, Troglobitic, Geophylogeny
 |
| Ancestral character state reconstruction using stochastic character mapping for the eye-trait morphology (Blind, Micro and Normal-eyed morphs) on a time calibrated phylogeny of using a “standard clock” estimate. A, B, C and D are four major clades. Posterior probabilities of node support values of 100% are indicated by *. Key events of Sinocyclocheilus evolution includes; at least three independent evolutionary events for Blind morphs; Blind, Micro-eyed and a few Normal-eyed species in Clade B, with two cases of reversal from either Micro-eyed or Blind to Normal-eyed species. Sinocyclocheilus diversification seems to have initiated in the mid-Miocene with the aridification of China |
 |
| a A specimen of Sinocyclocheilus altishoulderus indicating the position of 15 landmarks (red: larger points indicated by numbers 1–15) and 180 semi-landmarks (Orange: smaller point) used for the calculation of Procrustes coordinates and traditional linear measurements (SL standard length, ED eye diameter and sED standardized eye diameter) used in the geometric morphometric analyses. b PCA showing the variation in body shape of the genus Sinocyclocheilus traced with eye morphology, habitat occupation, existence of horn. PC1 and PC2 accounts for 32% and 17% of the variance respectively. A shift from the fusiform shape of the Normal-eyed surface forms to a more “boxy” form of the Micro-eyed and Blind forms is evident |
 |
| PCA showing the variation in body shape of the genus Sinocyclocheilus traced with eye morphology, habitat occupation, existence of horn. PC1 and PC2 accounts for 32% and 17% of the variance respectively. A shift from the fusiform shape of the Normal-eyed surface forms to a more “boxy” form of the Micro-eyed and Blind forms is evident |
Ting-Ru Mao, Ye-Wei Liu, Madhava Meegaskumbura, Jian Yang, Gajaba Ellepola, Gayani Senevirathne, Cheng-Hai Fu, Joshua B. Gross and Marcio R. Pie. 2021. Evolution in Sinocyclocheilus Cavefish is marked by Rate Shifts, Reversals, and Origin of Novel Traits.
BMC Ecology and Evolution. 21, 45. DOI: 10.1186/s12862-021-01776-y
