Evidence for nonallopatric speciation among closely related sympatric Heliotropium species in the Atacama Desert

Federico Luebert,Pit Jacobs,Ludo A H Muller,Hartmut H Hilger

doi:10.1002/ece3.929

Federico Luebert, Pit Jacobs + Show 2 more

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https://doi.org/10.1002/ece3.929

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Abstract

The genetic structure of populations of closely related, sympatric species may hold the signature of the geographical mode of the speciation process. In fully allopatric speciation, it is expected that genetic differentiation between species is homogeneously distributed across the genome. In nonallopatric speciation, the genomes may remain undifferentiated to a large extent. In this article, we analyzed the genetic structure of five sympatric species from the plant genus Heliotropium in the Atacama Desert. We used amplified fragment length polymorphisms (AFLPs) to characterize the genetic structure of these species and evaluate their genetic differentiation as well as the number of loci subject to positive selection using divergence outlier analysis (DOA). The five species form distinguishable groups in the genetic space, with zones of overlap, indicating that they are possibly not completely isolated. Among-species differentiation accounts for 35% of the total genetic differentiation (FST = 0.35), and FST between species pairs is positively correlated with phylogenetic distance. DOA suggests that few loci are subject to positive selection, which is in line with a scenario of nonallopatric speciation. These results support the idea that sympatric species of Heliotropium sect. Cochranea are under an ongoing speciation process, characterized by a fluctuation of population ranges in response to pulses of arid and humid periods during Quaternary times.

Highlights

Based on the spatial segregation of the involved populations, three major geographical categories have traditionally been recognized for the process of speciation
Classification of the speciation process into the discrete allopatric, parapatric, and sympatric modes is considered an oversimplification by several authors who have argued that speciation studies should focus on modeling and estimating parameters that describe the diversification process rather than on classifying the speciation mode according to geographical criteria (e.g., Wu 2001; Butlin et al 2008; Fitzpatrick et al 2008; Coyne 2011)
Amplified fragment length polymorphism analysis of 96 specimens belonging to five different Heliotropium species with three different selective PCR amplifications generated a total of 311 scorable loci, 287 (92%) of which were polymorphic across the whole set of samples

Summary

Introduction

Based on the spatial segregation of the involved populations, three major geographical categories have traditionally been recognized for the process of speciation. In the case of allopatric speciation, geographically isolated populations differentiate into distinct species and the speciation event occurs in the absence of gene flow. On the other hand, is a process that occurs in a single (geographical) population and in the presence of gene flow. Besides these two extreme forms of spatial segregation, partial segregation of the diverging populations can occur. The diversification of such populations with adjacent geographical ranges into distinct species, despite limited interbreeding at their contact zone, characterizes the process of parapatric speciation.

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