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New mitochondrial and nuclear evidences support recent demographic expansion and an atypical phylogeographic pattern in the spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae).

Rodrigues AS, Silva SE, Marabuto E, Silva DN, Wilson MR, Thompson V, Yurtsever S, Halkka A, Borges PA, Quartau JA, Paulo OS, Seabra SG - PLoS ONE (2014)

Bottom Line: Unexpected patterns of recent gene-flow events between Mediterranean peninsulas, a close relationship between Iberia and North Africa, as well as high levels of genetic diversity being maintained in northern Europe were found.The mitochondrial pattern does not exactly match to the nuclear pattern suggesting that the current biogeographic pattern of P. spumarius may be the result of both secondary admixture and incomplete lineage sorting.The hypothesis of recent colonization of North America from both western and northern Europe is corroborated by our data and probably resulted from accidental human translocations.

View Article: PubMed Central - PubMed

Affiliation: Computational Biology and Population Genomics Group, Centro de Biologia Ambiental, Departamento de Biologia Animal/Platform for Enhancing Ecological Research & Sustainability, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal.

ABSTRACT
Philaenus spumarius is a widespread insect species in the Holarctic region. Here, by focusing on the mtDNA gene COI but also using the COII and Cyt b genes and the nuclear gene EF-1α, we tried to explain how and when its current biogeographic pattern evolved by providing time estimates of the main demographic and evolutionary events and investigating its colonization patterns in and out of Eurasia. Evidence of recent divergence and expansion events at less than 0.5 Ma ago indicate that climate fluctuations in the Mid-Late Pleistocene were important in shaping the current phylogeographic pattern of the species. Data support a first split and differentiation of P. spumarius into two main mitochondrial lineages: the "western", in the Mediterranean region and the "eastern", in Anatolia/Caucasus. It also supports a following differentiation of the "western" lineage into two sub-lineages: the "western-Mediterranean", in Iberia and the "eastern-Mediterranean" in the Balkans. The recent pattern seems to result from postglacial range expansion from Iberia and Caucasus/Anatolia, thus not following one of the four common paradigms. Unexpected patterns of recent gene-flow events between Mediterranean peninsulas, a close relationship between Iberia and North Africa, as well as high levels of genetic diversity being maintained in northern Europe were found. The mitochondrial pattern does not exactly match to the nuclear pattern suggesting that the current biogeographic pattern of P. spumarius may be the result of both secondary admixture and incomplete lineage sorting. The hypothesis of recent colonization of North America from both western and northern Europe is corroborated by our data and probably resulted from accidental human translocations. A probable British origin for the populations of the Azores and New Zealand was revealed, however, for the Azores the distribution of populations in high altitude native forests is somewhat puzzling and may imply a natural colonization of the archipelago.

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Median-joining haplotype network of Philaenus spumarius sampled geographic regions for mitochondrial gene COI (539bp).Size of the circles is in proportion to the number of haplotypes. Branches begin in the centre of the circles and their sizes are in proportion to the number of mutations.
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pone-0098375-g003: Median-joining haplotype network of Philaenus spumarius sampled geographic regions for mitochondrial gene COI (539bp).Size of the circles is in proportion to the number of haplotypes. Branches begin in the centre of the circles and their sizes are in proportion to the number of mutations.

Mentions: Phylogenetic trees obtained for concatenated mtDNA genes and for a subset of P. spumarius individuals by the three methods, MP, ML and BI, presented a congruent topology. Maximum likelihood (Fig. 2), MP (not shown) and BI (not shown) trees, revealed the existence of two main haplotype groups: the “western” and the “eastern”. The “western” is divided in the “western-Mediterranean” and the “eastern-Mediterranean” sub-groups. The same phylogeographic pattern was found in the COI median-joining haplotype network (Fig. 3) and also in the COII and Cyt b median-joining haplotype networks (Fig. S1 and S2). The “eastern” haplogroup includes haplotypes from a wide geographical area, including northern Anatolia (Cerkes), Finland, Belgium, the UK (Aberdare – Wales) and eastern North America (New Hampshire – USA). In the “western-Mediterranean” group, the most common haplotype (H29) and several derived haplotypes, differing by one or two mutational steps, are shared between populations from the Iberian Peninsula, Morocco, France, Belgium, Italian Peninsula, Sicily and one individual from Balkans (H18). A group of haplotypes derived from H29 (H23, H24, H25, H70 and H71) includes samples from the Azores, western North America (British Columbia – Canada), eastern North America (Michigan – USA) and the UK, differing by two or three mutations. In the “eastern-Mediterranean” group, a similar star-like pattern is present with rare haplotypes connected to the most common (H57), usually by one mutational step. This group encompasses populations from the Balkans (Greece, Bulgaria and European Turkey), Slovenia, Italian Peninsula and Sicily. This lineage is also present in five samples from the eastern part of the Iberian Peninsula (H56) (Figs. 1 and 2).


New mitochondrial and nuclear evidences support recent demographic expansion and an atypical phylogeographic pattern in the spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae).

Rodrigues AS, Silva SE, Marabuto E, Silva DN, Wilson MR, Thompson V, Yurtsever S, Halkka A, Borges PA, Quartau JA, Paulo OS, Seabra SG - PLoS ONE (2014)

Median-joining haplotype network of Philaenus spumarius sampled geographic regions for mitochondrial gene COI (539bp).Size of the circles is in proportion to the number of haplotypes. Branches begin in the centre of the circles and their sizes are in proportion to the number of mutations.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043774&req=5

pone-0098375-g003: Median-joining haplotype network of Philaenus spumarius sampled geographic regions for mitochondrial gene COI (539bp).Size of the circles is in proportion to the number of haplotypes. Branches begin in the centre of the circles and their sizes are in proportion to the number of mutations.
Mentions: Phylogenetic trees obtained for concatenated mtDNA genes and for a subset of P. spumarius individuals by the three methods, MP, ML and BI, presented a congruent topology. Maximum likelihood (Fig. 2), MP (not shown) and BI (not shown) trees, revealed the existence of two main haplotype groups: the “western” and the “eastern”. The “western” is divided in the “western-Mediterranean” and the “eastern-Mediterranean” sub-groups. The same phylogeographic pattern was found in the COI median-joining haplotype network (Fig. 3) and also in the COII and Cyt b median-joining haplotype networks (Fig. S1 and S2). The “eastern” haplogroup includes haplotypes from a wide geographical area, including northern Anatolia (Cerkes), Finland, Belgium, the UK (Aberdare – Wales) and eastern North America (New Hampshire – USA). In the “western-Mediterranean” group, the most common haplotype (H29) and several derived haplotypes, differing by one or two mutational steps, are shared between populations from the Iberian Peninsula, Morocco, France, Belgium, Italian Peninsula, Sicily and one individual from Balkans (H18). A group of haplotypes derived from H29 (H23, H24, H25, H70 and H71) includes samples from the Azores, western North America (British Columbia – Canada), eastern North America (Michigan – USA) and the UK, differing by two or three mutations. In the “eastern-Mediterranean” group, a similar star-like pattern is present with rare haplotypes connected to the most common (H57), usually by one mutational step. This group encompasses populations from the Balkans (Greece, Bulgaria and European Turkey), Slovenia, Italian Peninsula and Sicily. This lineage is also present in five samples from the eastern part of the Iberian Peninsula (H56) (Figs. 1 and 2).

Bottom Line: Unexpected patterns of recent gene-flow events between Mediterranean peninsulas, a close relationship between Iberia and North Africa, as well as high levels of genetic diversity being maintained in northern Europe were found.The mitochondrial pattern does not exactly match to the nuclear pattern suggesting that the current biogeographic pattern of P. spumarius may be the result of both secondary admixture and incomplete lineage sorting.The hypothesis of recent colonization of North America from both western and northern Europe is corroborated by our data and probably resulted from accidental human translocations.

View Article: PubMed Central - PubMed

Affiliation: Computational Biology and Population Genomics Group, Centro de Biologia Ambiental, Departamento de Biologia Animal/Platform for Enhancing Ecological Research & Sustainability, Faculdade de Ciências, Universidade de Lisboa, Lisboa, Portugal.

ABSTRACT
Philaenus spumarius is a widespread insect species in the Holarctic region. Here, by focusing on the mtDNA gene COI but also using the COII and Cyt b genes and the nuclear gene EF-1α, we tried to explain how and when its current biogeographic pattern evolved by providing time estimates of the main demographic and evolutionary events and investigating its colonization patterns in and out of Eurasia. Evidence of recent divergence and expansion events at less than 0.5 Ma ago indicate that climate fluctuations in the Mid-Late Pleistocene were important in shaping the current phylogeographic pattern of the species. Data support a first split and differentiation of P. spumarius into two main mitochondrial lineages: the "western", in the Mediterranean region and the "eastern", in Anatolia/Caucasus. It also supports a following differentiation of the "western" lineage into two sub-lineages: the "western-Mediterranean", in Iberia and the "eastern-Mediterranean" in the Balkans. The recent pattern seems to result from postglacial range expansion from Iberia and Caucasus/Anatolia, thus not following one of the four common paradigms. Unexpected patterns of recent gene-flow events between Mediterranean peninsulas, a close relationship between Iberia and North Africa, as well as high levels of genetic diversity being maintained in northern Europe were found. The mitochondrial pattern does not exactly match to the nuclear pattern suggesting that the current biogeographic pattern of P. spumarius may be the result of both secondary admixture and incomplete lineage sorting. The hypothesis of recent colonization of North America from both western and northern Europe is corroborated by our data and probably resulted from accidental human translocations. A probable British origin for the populations of the Azores and New Zealand was revealed, however, for the Azores the distribution of populations in high altitude native forests is somewhat puzzling and may imply a natural colonization of the archipelago.

Show MeSH
Related in: MedlinePlus