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

Lawson LP, Bates JM, Menegon M, Loader SP - BMC Evol. Biol. (2015)

Bottom Line: An associated climate shift was observed in most potentially peripatric splits.The potentially allopatric species pair showed no niche shifts and equivalent effective population sizes, ruling out peripatry in that speciation event.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.

View Article: PubMed Central - PubMed

Affiliation: Committee on Evolutionary Biology, University of Chicago, 1025 E. 57th St. Culver Hall 402, Chicago, IL, 60637, USA. lucinda.lawson@uc.edu.

ABSTRACT

Background: Peripatric 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.

Results: We 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).

Conclusions: In 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.

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EBSP plots of effective population sizes and potential bottlenecks in populations and species with largest sample sizes. a-d show single mountain block populations within species. aH. minutissimus population in the Udzungwa Mountains. bH. burgessi in the East Usambara Mountains. cH. burgessi on Malundwe Hill. dH. burgessi in the Nguru Mountains. e-g show all descendent individuals from deeper phylogenetic nodes
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Fig3: EBSP plots of effective population sizes and potential bottlenecks in populations and species with largest sample sizes. a-d show single mountain block populations within species. aH. minutissimus population in the Udzungwa Mountains. bH. burgessi in the East Usambara Mountains. cH. burgessi on Malundwe Hill. dH. burgessi in the Nguru Mountains. e-g show all descendent individuals from deeper phylogenetic nodes

Mentions: No populations showed signs of ancestral bottlenecks or expansions, though the narrowly distributed species (H. tanneri, H. ukwiva, H. davenporti; distributions in Table 3) did not have sufficient sample sizes to analyze Extended Bayesian Skyline Plots (EBSP). In EBSP plots, most populations showed potential current bottlenecks, which may be related to recent range reductions of habitats due to climatic and/or anthropogenic events (Fig. 3). Only the population of H. burgessi in the East Usambara Mountains does not appear to show a current reduction, though this is also the population with greatest sampling. EBSP plots of all individuals from deeper nodes did not show bottlenecks or expansions except when including all individuals from all species, which shows an expansion beginning around 8 MYA that peaks around 4 MYA. This coincides with the split between H. tanneri and the H. spinigularis/burgessi/davenporti clade.Table 3


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

Lawson LP, Bates JM, Menegon M, Loader SP - BMC Evol. Biol. (2015)

EBSP plots of effective population sizes and potential bottlenecks in populations and species with largest sample sizes. a-d show single mountain block populations within species. aH. minutissimus population in the Udzungwa Mountains. bH. burgessi in the East Usambara Mountains. cH. burgessi on Malundwe Hill. dH. burgessi in the Nguru Mountains. e-g show all descendent individuals from deeper phylogenetic nodes
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4487588&req=5

Fig3: EBSP plots of effective population sizes and potential bottlenecks in populations and species with largest sample sizes. a-d show single mountain block populations within species. aH. minutissimus population in the Udzungwa Mountains. bH. burgessi in the East Usambara Mountains. cH. burgessi on Malundwe Hill. dH. burgessi in the Nguru Mountains. e-g show all descendent individuals from deeper phylogenetic nodes
Mentions: No populations showed signs of ancestral bottlenecks or expansions, though the narrowly distributed species (H. tanneri, H. ukwiva, H. davenporti; distributions in Table 3) did not have sufficient sample sizes to analyze Extended Bayesian Skyline Plots (EBSP). In EBSP plots, most populations showed potential current bottlenecks, which may be related to recent range reductions of habitats due to climatic and/or anthropogenic events (Fig. 3). Only the population of H. burgessi in the East Usambara Mountains does not appear to show a current reduction, though this is also the population with greatest sampling. EBSP plots of all individuals from deeper nodes did not show bottlenecks or expansions except when including all individuals from all species, which shows an expansion beginning around 8 MYA that peaks around 4 MYA. This coincides with the split between H. tanneri and the H. spinigularis/burgessi/davenporti clade.Table 3

Bottom Line: An associated climate shift was observed in most potentially peripatric splits.The potentially allopatric species pair showed no niche shifts and equivalent effective population sizes, ruling out peripatry in that speciation event.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.

View Article: PubMed Central - PubMed

Affiliation: Committee on Evolutionary Biology, University of Chicago, 1025 E. 57th St. Culver Hall 402, Chicago, IL, 60637, USA. lucinda.lawson@uc.edu.

ABSTRACT

Background: Peripatric 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.

Results: We 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).

Conclusions: In 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.

Show MeSH
Related in: MedlinePlus