Genetic and morphological support for possible sympatric origin of fish from subterranean habitats

Iraj Hashemzadeh Segherloo,Nabiallah Ghaedrahmati,Asghar Abdoli,Clément Rougeux,Eric Normandeau,Guillaume Coté,Jean-Sébastien Moore,Laura Benestan,Louis Bernatchez

doi:10.1038/s41598-018-20666-w

Iraj Hashemzadeh Segherloo, Nabiallah Ghaedrahmati + Show 7 more

Open Access

https://doi.org/10.1038/s41598-018-20666-w

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Abstract

Two blind Iran cave barbs, Garra typhlops and Garra lorestanensis, exist in sympatry in a single subterranean habitat, raising the hypothesis that they may represent a case of sympatric speciation following a colonization event. Their different mental disc forms have prompted some authors to propose the alternative hypothesis of two separate colonization events. In this study, we analysed a genome-wide panel of 11,257 SNPs genotyped by means of genotyping-by-sequencing combined with mitochondrial cytochrome c oxidase sub-unit I sequence data, field observations and morphological traits to test these two hypotheses. Field data suggest some degree of ecological divergence despite some possible niche overlap such that hybridization is possible. According to both nuclear and mtDNA data, the cave barb species are monophyletic with close phylogenetic relationships with Garra gymnothorax from the Karun-Dez and Karkheh river basins. The historical demography analysis revealed that a model of Isolation-with-Migration (IM) best fitted the data, therefore better supporting a scenario of sympatric origin than that of allopatric isolation followed by secondary contact. Overall, our results offer stronger support to the hypothesis that speciation in the subterranean habitat could have occurred in sympatry following a colonization event from the Karun-Dez-Karkheh basins in the Zagros Mountains of Iran.

Highlights

Speciation is the keystone process of diversification and can be categorized in geographic and non-geographic modes
The G. typhlops and G. lorestanensis groups were completely separated on the discriminant function plot
The positioning of the mouth opening is nearly terminal in G. thyphlops and the intermediate form compared to G. lorestanensis (Fig. 2a and b)

Summary

Introduction

Speciation is the keystone process of diversification and can be categorized in geographic and non-geographic modes. Subterranean habitats are environmentally stable (e.g., stable temperature, darkness), but limited in trophic resources and primary production due to low light intensity resulting in a low rate of photosynthesis[11,12,13] This light limitation, jointly with an eco-hydraulic zonation of subterranean habitats[11], makes them an excellent natural context to study the evolution of biodiversity[13]. These features of the subterranean habitats increase the intensity of competition for limited resources and can lead to species/population divergence to maximize the use of variable resources and habitat types while minimizing competition[5,12] This diversification in habitat use can drive reproductive isolation and sympatric speciation. We have recently observed an individual exhibiting an intermediate disc form in the cave barb locality that may be a hybrid, an extreme case of intra-specific variation, or a genetically differentiated species

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