Genomic methods reveal independent demographic histories despite strong morphological conservatism in fish species

Jessika M M Neves,Nidia N Fabré,Zachary J Nolen,Ricardo J Pereira,Tamí Mott

doi:10.1038/s41437-021-00455-4

Jessika M M Neves, Nidia N Fabré + Show 3 more

Open Access

https://doi.org/10.1038/s41437-021-00455-4

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Abstract

Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies, especially in regards to highly vulnerable marine ecosystems. In this context, cryptic species are particularly challenging to conserve because they are hard to distinguish based on morphology alone, and thus it is often unclear how many species coexist in sympatry, what are their phylogenetic relationships and their demographic history. We answer these questions using morphologically similar species of the genus Mugil that are sympatric in the largest coastal Marine Protected Area in the Tropical Southwestern Atlantic marine province. Using a sub-representation of the genome, we show that individuals are assigned to five highly differentiated genetic clusters that are coincident with five mitochondrial lineages, but discordant with morphological information, supporting the existence of five species with conserved morphology in this region. A lack of admixed individuals is consistent with strong genetic isolation between sympatric species, but the most likely species tree suggests that in one case speciation has occurred in the presence of interspecific gene flow. Patterns of genetic diversity within species suggest that effective population sizes differ up to two-fold, probably reflecting differences in the magnitude of population expansions since species formation. Together, our results show that strong morphologic conservatism in marine environments can lead to species that are difficult to distinguish morphologically but that are characterized by an independent evolutionary history, and thus that deserve species-specific management strategies.

Highlights

Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies (Mora and Zapata 2013)
Designing sustainable and science-based measures for managing wild populations requires a fundamental knowledge on the number of species, their genetic connectivity, diversity, and demographic history (Scott et al 2020; Bilgmann et al 2021; Hoffmann et al 2021)
We use a genomic approach to resolve these evolutionary questions and understand how speciation of these morphologically similar species can lead to the maintenance of strong genetic isolation in the absence of geographic isolation

Summary

Introduction

Human overexploitation of natural resources has placed conservation and management as one of the most pressing challenges in modern societies (Mora and Zapata 2013). Understanding the number and distribution of morphologically cryptic species has strongly benefited from studying fast evolving mitochondrial genes, which are revealing an exponentially growing number of species (Sáez and Lozano 2005), and their demographic history (Carnaval et al 2009). Such discoveries of hidden genetic diversity have been reported even in previously known biodiversity hotspots, such as in the Amazon (Benzaquem et al 2015), and in marine ecosystems (Asgharian et al 2011; Brandão et al 2016). Assessing the phylogenetic relationships between sympatric cryptic species, their levels of genetic connectivity, and their demographic history offer important insights into the process of species formation

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