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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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Ecological Niche Divergence of speciation according to major habitat types. Left: Principle Component Analysis of current habitat suitability for each species. Montane grassland/forest mosaic species are on the right, while rainforest adapted species are on the left. Right: Distribution of forest (trees) and mosaic (grasses) adapted species on *BEAST species tree. A double-sided arrow between habitat types indicates the two nodes where ecological shifts are inferred. Relative population sizes based on field collection estimates and potential range sizes are shown in the relative size of color-key circles. The split distribution of H. spinigularis is represented by two circles to represent the two distant populations in Malawi and Mozambique separated by ~160 km. The two localities of H. tanneri are represented by a single circle as they are within the same mountain block and separated by only ~25 km
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Fig5: Ecological Niche Divergence of speciation according to major habitat types. Left: Principle Component Analysis of current habitat suitability for each species. Montane grassland/forest mosaic species are on the right, while rainforest adapted species are on the left. Right: Distribution of forest (trees) and mosaic (grasses) adapted species on *BEAST species tree. A double-sided arrow between habitat types indicates the two nodes where ecological shifts are inferred. Relative population sizes based on field collection estimates and potential range sizes are shown in the relative size of color-key circles. The split distribution of H. spinigularis is represented by two circles to represent the two distant populations in Malawi and Mozambique separated by ~160 km. The two localities of H. tanneri are represented by a single circle as they are within the same mountain block and separated by only ~25 km

Mentions: PCA analysis of full and reduced bioclim variables (19 vs. 7) showed equivalent patterns, and thus only the reduced dataset is discussed. Two major clades of species were identified along PC1 marking the split between a rainforest adapted group (H. burgessi, H. tanneri, and H. spinigularis) and a mosaic-adapted group (H. ukwiva, H. minutissimus, and H. davenporti) (non-overlapping 95 % confidence intervals; Fig. 5, Additional file 2: Table S4). PC1 (53 % explained variance) is dominated by the temperature and precipitation during the coldest and driest times of year. These habitat syndromes, when mapped onto the phylogenetic tree, show two major adaptive habitat shifts to high elevation grasslands (Fig. 5), presuming that the ancestor was forest-adapted in line with paleoclimatic estimates of conditions ~ 4 MYA [50], before a general shift to grasslands at 1.86 MYA [51].Fig. 5


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)

Ecological Niche Divergence of speciation according to major habitat types. Left: Principle Component Analysis of current habitat suitability for each species. Montane grassland/forest mosaic species are on the right, while rainforest adapted species are on the left. Right: Distribution of forest (trees) and mosaic (grasses) adapted species on *BEAST species tree. A double-sided arrow between habitat types indicates the two nodes where ecological shifts are inferred. Relative population sizes based on field collection estimates and potential range sizes are shown in the relative size of color-key circles. The split distribution of H. spinigularis is represented by two circles to represent the two distant populations in Malawi and Mozambique separated by ~160 km. The two localities of H. tanneri are represented by a single circle as they are within the same mountain block and separated by only ~25 km
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Ecological Niche Divergence of speciation according to major habitat types. Left: Principle Component Analysis of current habitat suitability for each species. Montane grassland/forest mosaic species are on the right, while rainforest adapted species are on the left. Right: Distribution of forest (trees) and mosaic (grasses) adapted species on *BEAST species tree. A double-sided arrow between habitat types indicates the two nodes where ecological shifts are inferred. Relative population sizes based on field collection estimates and potential range sizes are shown in the relative size of color-key circles. The split distribution of H. spinigularis is represented by two circles to represent the two distant populations in Malawi and Mozambique separated by ~160 km. The two localities of H. tanneri are represented by a single circle as they are within the same mountain block and separated by only ~25 km
Mentions: PCA analysis of full and reduced bioclim variables (19 vs. 7) showed equivalent patterns, and thus only the reduced dataset is discussed. Two major clades of species were identified along PC1 marking the split between a rainforest adapted group (H. burgessi, H. tanneri, and H. spinigularis) and a mosaic-adapted group (H. ukwiva, H. minutissimus, and H. davenporti) (non-overlapping 95 % confidence intervals; Fig. 5, Additional file 2: Table S4). PC1 (53 % explained variance) is dominated by the temperature and precipitation during the coldest and driest times of year. These habitat syndromes, when mapped onto the phylogenetic tree, show two major adaptive habitat shifts to high elevation grasslands (Fig. 5), presuming that the ancestor was forest-adapted in line with paleoclimatic estimates of conditions ~ 4 MYA [50], before a general shift to grasslands at 1.86 MYA [51].Fig. 5

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