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Global biogeography and evolution of Cuvierina pteropods.

Burridge AK, Goetze E, Raes N, Huisman J, Peijnenburg KT - BMC Evol. Biol. (2015)

Bottom Line: We found evidence for ecological differentiation among all morphotypes based on ecological niche modelling with sea surface temperature, salinity and phytoplankton biomass as primary determinants.Across all analyses, we found highly congruent patterns of differentiation suggesting species level divergences between morphotypes.However, we also found distinct morphotypes (e.g. in the Atlantic Ocean) that were ecologically, but not genetically differentiated.

View Article: PubMed Central - PubMed

Affiliation: Naturalis Biodiversity Center, P.O. Box 9517, Leiden, 2300 RA, The Netherlands. Alice.Burridge@naturalis.nl.

ABSTRACT

Background: Shelled pteropods are planktonic gastropods that are potentially good indicators of the effects of ocean acidification. They also have high potential for the study of zooplankton evolution because they are metazoan plankton with a good fossil record. We investigated phenotypic and genetic variation in pteropods belonging to the genus Cuvierina in relation to their biogeographic distribution across the world's oceans. We aimed to assess species boundaries and to reconstruct their evolutionary history.

Results: We distinguished six morphotypes based on geometric morphometric analyses of shells from 926 museum and 113 fresh specimens. These morphotypes have distinct geographic distributions across the Atlantic, Pacific and Indian oceans, and belong to three major genetic clades based on COI and 28S DNA sequence data. Using a fossil-calibrated phylogeny, we estimated that these clades separated in the Late Oligocene and Early to Middle Miocene. We found evidence for ecological differentiation among all morphotypes based on ecological niche modelling with sea surface temperature, salinity and phytoplankton biomass as primary determinants. Across all analyses, we found highly congruent patterns of differentiation suggesting species level divergences between morphotypes. However, we also found distinct morphotypes (e.g. in the Atlantic Ocean) that were ecologically, but not genetically differentiated.

Conclusions: Given the distinct ecological and phenotypic specializations found among both described and undescribed Cuvierina taxa, they may not respond equally to future ocean changes and may not be equally sensitive to ocean acidification. Our findings support the view that ecological differentiation may be an important driving force in the speciation of zooplankton.

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Unrooted maximum likelihood tree of 136 Cytochrome Oxidase I gene sequences ofCuvierina. Three sequences are from GenBank: FJ876895, Atlantic; FJ876896-7, Indian Ocean. Numbers indicate bootstrap support (only bootstrap values of major clades are shown). Symbols indicate major genetic clades; colours indicate distinct morphotypes (also see Figure 5).
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Fig4: Unrooted maximum likelihood tree of 136 Cytochrome Oxidase I gene sequences ofCuvierina. Three sequences are from GenBank: FJ876895, Atlantic; FJ876896-7, Indian Ocean. Numbers indicate bootstrap support (only bootstrap values of major clades are shown). Symbols indicate major genetic clades; colours indicate distinct morphotypes (also see Figure 5).

Mentions: We found high levels of mitochondrial diversity in a data set of 136 COI sequences collected from global samples of Cuvierina, including 127 different haplotypes represented by 166 polymorphic sites (GenBank accession numbers KP292656–KP292788; Additional file 1). We translated COI sequences into amino acids and discarded the possibility of pseudogenes because we found no stop codons and no insertions or deletions. Phylogenetic analysis of COI sequences indicated the presence of three major mitochondrial clades (Figure 4 and Additional file 3). These three monophyletic clades were highly supported (bootstrap values of 84–99%) are largely congruent with morphotypes as well as geographic distributions (Figure 5). The three major clades were named after their geographic distributions; viz., Atlantic, Indo-Pacific and South Pacific (Figures 4 and 5). The Atlantic clade contains both the C. atlantica and C. cancapae morphotypes: we did not find any grouping of these morphotypes, nor did we find any grouping of individuals from either the North or South Atlantic. The Indo-Pacific clade consists of C. urceolaris, C. pacifica N and C. columnella morphotypes. Within this clade, C. pacifica N was paraphyletic. Our single specimen of the C. urceolaris morphotype grouped with two GenBank sequences from the Indian Ocean (both reported as C. columnella, [32]). The South Pacific clade consists entirely of the C. pacifica S morphotype. Average pairwise genetic distances of COI were 4.5–5.1% between major clades and 2.0%, 1.7% and 0.8% within clades for the Atlantic, Indo-Pacific and South Pacific, respectively (Additional file 4).Figure 4


Global biogeography and evolution of Cuvierina pteropods.

Burridge AK, Goetze E, Raes N, Huisman J, Peijnenburg KT - BMC Evol. Biol. (2015)

Unrooted maximum likelihood tree of 136 Cytochrome Oxidase I gene sequences ofCuvierina. Three sequences are from GenBank: FJ876895, Atlantic; FJ876896-7, Indian Ocean. Numbers indicate bootstrap support (only bootstrap values of major clades are shown). Symbols indicate major genetic clades; colours indicate distinct morphotypes (also see Figure 5).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4443520&req=5

Fig4: Unrooted maximum likelihood tree of 136 Cytochrome Oxidase I gene sequences ofCuvierina. Three sequences are from GenBank: FJ876895, Atlantic; FJ876896-7, Indian Ocean. Numbers indicate bootstrap support (only bootstrap values of major clades are shown). Symbols indicate major genetic clades; colours indicate distinct morphotypes (also see Figure 5).
Mentions: We found high levels of mitochondrial diversity in a data set of 136 COI sequences collected from global samples of Cuvierina, including 127 different haplotypes represented by 166 polymorphic sites (GenBank accession numbers KP292656–KP292788; Additional file 1). We translated COI sequences into amino acids and discarded the possibility of pseudogenes because we found no stop codons and no insertions or deletions. Phylogenetic analysis of COI sequences indicated the presence of three major mitochondrial clades (Figure 4 and Additional file 3). These three monophyletic clades were highly supported (bootstrap values of 84–99%) are largely congruent with morphotypes as well as geographic distributions (Figure 5). The three major clades were named after their geographic distributions; viz., Atlantic, Indo-Pacific and South Pacific (Figures 4 and 5). The Atlantic clade contains both the C. atlantica and C. cancapae morphotypes: we did not find any grouping of these morphotypes, nor did we find any grouping of individuals from either the North or South Atlantic. The Indo-Pacific clade consists of C. urceolaris, C. pacifica N and C. columnella morphotypes. Within this clade, C. pacifica N was paraphyletic. Our single specimen of the C. urceolaris morphotype grouped with two GenBank sequences from the Indian Ocean (both reported as C. columnella, [32]). The South Pacific clade consists entirely of the C. pacifica S morphotype. Average pairwise genetic distances of COI were 4.5–5.1% between major clades and 2.0%, 1.7% and 0.8% within clades for the Atlantic, Indo-Pacific and South Pacific, respectively (Additional file 4).Figure 4

Bottom Line: We found evidence for ecological differentiation among all morphotypes based on ecological niche modelling with sea surface temperature, salinity and phytoplankton biomass as primary determinants.Across all analyses, we found highly congruent patterns of differentiation suggesting species level divergences between morphotypes.However, we also found distinct morphotypes (e.g. in the Atlantic Ocean) that were ecologically, but not genetically differentiated.

View Article: PubMed Central - PubMed

Affiliation: Naturalis Biodiversity Center, P.O. Box 9517, Leiden, 2300 RA, The Netherlands. Alice.Burridge@naturalis.nl.

ABSTRACT

Background: Shelled pteropods are planktonic gastropods that are potentially good indicators of the effects of ocean acidification. They also have high potential for the study of zooplankton evolution because they are metazoan plankton with a good fossil record. We investigated phenotypic and genetic variation in pteropods belonging to the genus Cuvierina in relation to their biogeographic distribution across the world's oceans. We aimed to assess species boundaries and to reconstruct their evolutionary history.

Results: We distinguished six morphotypes based on geometric morphometric analyses of shells from 926 museum and 113 fresh specimens. These morphotypes have distinct geographic distributions across the Atlantic, Pacific and Indian oceans, and belong to three major genetic clades based on COI and 28S DNA sequence data. Using a fossil-calibrated phylogeny, we estimated that these clades separated in the Late Oligocene and Early to Middle Miocene. We found evidence for ecological differentiation among all morphotypes based on ecological niche modelling with sea surface temperature, salinity and phytoplankton biomass as primary determinants. Across all analyses, we found highly congruent patterns of differentiation suggesting species level divergences between morphotypes. However, we also found distinct morphotypes (e.g. in the Atlantic Ocean) that were ecologically, but not genetically differentiated.

Conclusions: Given the distinct ecological and phenotypic specializations found among both described and undescribed Cuvierina taxa, they may not respond equally to future ocean changes and may not be equally sensitive to ocean acidification. Our findings support the view that ecological differentiation may be an important driving force in the speciation of zooplankton.

Show MeSH