Rapid adaptive radiation in a hillstream cyprinid fish in the East African White Nile River basin

Abstract

Adaptive radiation of freshwater fishes was long thought to be possible only in lacustrine environments. Recently, several studies have shown that riverine and stream environments also provide the ecological opportunity for adaptive radiation. In this study, we report on a riverine adaptive radiation of six ecomorphs of cyprinid hillstream fishes of the genus Garra in a river located in the Ethiopian Highlands in East Africa. Garra are predominantly highly specialized algae-scrapers with a wide distribution ranging from Southeast Asia to West Africa. However, adaptive phenotypic diversification in mouth type, sucking disc morphology, gut length and body shape have probably been found among these ecomorphs in a single Ethiopian river. Moreover, we found two novel phenotypes of Garra ("thick-lipped" and "predatory") that had not been discovered before in this species-rich genus (>160 species). Mitochondrial and genome-wide data suggest monophyletic, intrabasin evolution of Garra phenotypic diversity with signatures of gene flow from other local populations. Although sympatric ecomorphs are genetically distinct and can be considered to being young species as suggested by genome-wide single nucleotide polymorphism data, mitochondrial DNA was unable to identify any genetic structure suggesting recent and rapid speciation events. Some data suggest a hybrid origin of the novel "thick-lipped" ecomorph.Here we highlight how, driven by ecological opportunity, an ancestral trophically highly specialized lineage is likely to have rapidly radiated in a riverine environment promoted by the evolution of novel feeding strategies.

Unexpected Diversity of Feeding Modes among Chisel-Mouthed Ethiopian Labeobarbus (Cyprinidae)

“…The evolution of periphytonophagous adaptations probably occurred over millions of years. Specialized lineages of periphitonophagous scrapers can be found among a type of Asian cyprinids of a rather old origin (Miocene), e.g., Capoeta (Valenciennes 1842), Cyprinion (Heckel 1843), Garra (Hamilton 1822), Onychostoma (Günther 1896), Scaphiodonichthys (Vinciguerra 1890), Schizothorax (Heckel 1838), Schizopygopsis (Steindachner 1866) [28,32,33]; however, note the exceptions in feeding specialization for some members of these genera [17,26,69]. In the case of chisel-mouthed fish, periphyton feeding is accompanied by morpho-ecological adaptations, such as modified jaws, a long gut with thin walls, increased gill raker numbers, and often a black peritoneum ( [27,45], this study).…”

“…In addition, the mid-upper reaches are characterized by the increased availability of ecological niches compared to the most-upper reach (i.e., more diverse ecotopes/habitats in this section offer more ecological opportunities, see [3]). The combination of these conditions (lower competition and diverse habitats) could promote adaptive radiation among the Ethiopian cyprinids [17].…”

“…Ecological diversification is a cornerstone of the process of adaptive radiation, considered as one of the main sources of biodiversity emergence [1][2][3][4]. The Ethiopian Highlands appears to be a hotspot of adaptive radiation in the cyprinid genera Labeobarbus, Enteromius and Garra, in both lacustrine and riverine environments [5][6][7][8][9][10][11][12][13][14][15][16][17]. Based on fish morphology, it was suggested that trophic resource partitioning was the main driver for these cyprinid radiations, and this has been proven for some lacustrine and riverine Labeobarbus assemblages [11,15].…”

A speciation continuum within repeated origin of hypertrophied lips in cyprinid fish from East Africa

“…Adaptive radiations based on trophic resource partitioning have been studied in fishes such as cichlids, coregonids, Arctic charr, three-spined sticklebacks, and many other lineages of fish (Skulason, Smith, 1995;Schluter, 2000;Sibbing, Nagelkerke, 2000;Barluenga et al, 2006;Martin and Wainwright, 2011;Seehausen and Wagner, 2014;Burress, 2016). Cyprinid fishes, Family Cyprinidae sensu lato , is one of the most diversified families of Actinopterygii (> 3000 species -Fricke et al, 2022) that contains many adaptive radiations (e.g., Kornfield, Karpenter, 1984;Savvaitova et al, 1987;Nagelkerke et al, 1994;Mina et al, 1996;Levin et al, 2020;2021a;Komarova et al, 2021), most of which, however, have not yet been studied using genome-wide approaches.…”

Speciation and repeated origins of hypertrophied lips in parallel adaptive radiations of cyprinid fish from East Africa

“…Adaptive radiations based on trophic resource partitioning have been studied in fishes, such as cichlids, coregonids, Arctic charr, three‐spined sticklebacks, and many other lineages of fish (Barluenga et al, 2006 ; Burress, 2016 ; Martin & Wainwright, 2011 ; Schluter, 2000 ; Seehausen & Wagner, 2014 ; Sibbing & Nagelkerke, 2000 ; Skulason & Smith, 1995 ). Cyprinid fishes, family Cyprinidae sensu lato , is one of the most diversified families of Actinopterygii (>3000 species – Fricke et al, 2022 ) that contains many adaptive radiations (e.g., Komarova et al, 2021 ; Kornfield & Carpenter, 1984 ; Levin et al, 2020 ; Levin, Simonov, et al, 2021 ; Mina et al, 1996 ; Nagelkerke et al, 1994 ; Savvaitova et al, 1987 ), most of which, however, have not yet been studied using genome‐wide approaches.…”