Divergence at the edges: peripatric isolation in the montane spiny throated reed frog complex.

Lucinda P Lawson,Simon P Loader,John M Bates,Michele Menegon

doi:10.1186/s12862-015-0384-3

Abstract

BackgroundPeripatric speciation and peripheral isolation have uncertain importance in species accumulation, and are largely overshadowed by assumed dominance of allopatric modes of speciation. Understanding the role of different speciation mechanisms within biodiversity hotspots is central to understanding the generation of biological diversity. Here, we use a phylogeographic analysis of the spiny-throated reed frogs and examine sister pairings with unbalanced current distributional ranges for characteristics of peripatric speciation. We further investigate whether forest/grassland mosaic adapted species are more likely created through peripatric speciation due to instability of this habitat type.ResultsWe reconstructed a multi-locus molecular phylogeny of spiny-throated reed frogs which we then combined with comparative morphologic data to delimit species and analyze historical demographic change; identifying three new species. Three potential peripatric speciation events were identified along with one case of allopatric speciation. Peripatric speciation is supported through uneven potential and realized distributions and uneven population size estimates based on field collections. An associated climate shift was observed in most potentially peripatric splits. Morphological variation was highest in sexually dimorphic traits such as body size and gular shape, but this variation was not limited to peripatric species pairs as hypothesized. The potentially allopatric species pair showed no niche shifts and equivalent effective population sizes, ruling out peripatry in that speciation event. Two major ecological niche shifts were recovered within this radiation, possibly as adaptations to occupy areas of grassland that became more prevalent in the last 5 million years. Restricted and fluctuating grassland mosaics within forests might promote peripatric speciation in the Eastern Arc Biodiversity Hotspot (EABH).ConclusionsIn our case study, peripatric speciation appears to be an important driver of diversity within the EABH biodiversity hotspot, implying it could be a significant speciation mechanism in highly fragmented ecosystems. Extensive peripatric speciation in this montane archipelago may explain the abundance of discrete lineages within the limited area of the EABH, as inferred in remote island archipelagos. Future phylogenetic studies incorporating demographic and spatial analyses will clarify the role of peripatric speciation in creating biodiversity hotspots.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0384-3) contains supplementary material, which is available to authorized users.

Highlights

Peripatric speciation and peripheral isolation have uncertain importance in species accumulation, and are largely overshadowed by assumed dominance of allopatric modes of speciation
All methods show monophyletic relationships supporting six lineages: the previously described species of H. tanneri and H. minutissimus, a new species from the Rubeho Mountains (H. ukwiva), three distinct lineages (H. spinigularis, H. davenporti, and H. burgessi) which once were lumped into a single species (H. spinigularis)
Specimens previously identified as H. spinigularis from the Udzungwa Mountains [48] were included in this analysis and all were definitively genetically and morphologically H. minutissimus, confirming earlier estimates that only H. minutissimus is found in the Udzungwa Mountain block

Summary

Introduction

Peripatric speciation and peripheral isolation have uncertain importance in species accumulation, and are largely overshadowed by assumed dominance of allopatric modes of speciation. Isolation has been historically considered the most frequent mechanism to limit gene flow, promoting divergence of lineages leading to speciation [1, 2]. Numerous examples have been cited demonstrating the process of allopatry in driving speciation (summarized in [3, 4]), and the signal of vicariant barriers limiting gene flow has been shown in many comparative phylogeographic studies [5,6,7,8]. A small population is isolated at the edge of a larger population and rapidly diversifies, often crossing a previous barrier to dispersal and/or occupying a newly available ecological niche/ habitat type. Parapatric speciation events involve a shift in habitat requirements or ecological niche, though unlike in peripatric speciation, there are no physical barriers separating divergent lineages. New analytical approaches using multiple types of data enable testing for these processes in greater detail [10,11,12,13]

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