Relationships of a new species support multiple origin of melanism in Trichomycterus from the Atlantic Forest of south-eastern Brazil (Siluriformes: Trichomycteridae)

Abstract

The origin of melanism has been often associated with cryptic habits, driven by selection for camouflage, sometimes independently arising in closely related species. Field studies in Atlantic Forest rivers of south-eastern Brazil have indicated the occurrence of three melanic species in the catfish genus Trichomycterus: Trichomycterus immaculatus, Trichomycterus nigricans, and T. quintus Costa sp. nov. We performed a molecular analysis using two nuclear and two mitochondrial genes (2811 bp) for 62 trichomycterines and eight outgroups, in which monophyly of a group here named as the T. nigricans-nigroauratus clade is highly supported. It comprises two subclades, the T. nigricans group (containing Trichomycterus caipora, T. immaculatus, T. nigricans, and Trichomycterus santaeritae) and the Trichomycterus nigroauratus group (containing Trichomycterus maculosus, T. nigroauratus, and T. quintus). Ancestral state reconstructions indicate that melanism has arisen independently in each species exhibiting overall black colouration, which may be favoured by the strict nocturnal habits of these three species. However, whereas in the T. nigricans group cryptic habits precede the origin of melanism, in the T. nigroauratus group these events occur simultaneously during the evolution of T. quintus. Two melanic species, T. immaculatus and T. quintus, are sympatric but inhabit different habitats, suggesting some ecological divergence. Oppositely to the crypsis evolutionary trend, the analysis indicates a reversal to diurnal habits in the psammophilic T. santaeritae. This species, uniquely among congeners of the T. nigricans-nigroauratus clade, has a colour pattern consisting of dark brown blotches on a pale yellow colour ground and relatively large eyes, allowing sandy habitat camouflage and visual orientation during foraging activity, respectively, interpreted as adaptive morphological changes parallelly found in other diurnal psammophilic trichomycterids.