In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricular... more In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula).
Nucleotide sequences of seven chloroplast (atpB and rbcL, SSU and LSU rDNAs), mitochondrial (atp1... more Nucleotide sequences of seven chloroplast (atpB and rbcL, SSU and LSU rDNAs), mitochondrial (atp1, LSU rDNA), and nuclear (18S rDNA) genes from 192 land plants and their algal relatives were analyzed using maximum likelihood and maximum parsimony ...
Proceedings of The National Academy of Sciences, 2004
Much recent attention in the study of adaptation of organismal form has centered on developmental... more Much recent attention in the study of adaptation of organismal form has centered on developmental regulation. As such, the highly conserved respiratory machinery of eukaryotic cells might seem an unlikely target for selection supporting novel morphologies. We demonstrate that a dramatic molecular evolutionary rate increase in subunit I of cytochrome c oxidase (COX) from an active-trapping lineage of carnivorous plants is caused by positive Darwinian selection. Bladderworts (Utricularia) trap plankton when water-immersed, negatively pressured suction bladders are triggered. The resetting of traps involves active ion transport, requiring considerable energy expenditure. As judged from the quaternary structure of bovine COX, the most profound adaptive substitutions are two contiguous cysteines absent in 99.9% of databased COX I sequences from Eukaryota, Archaea, and Bacteria. This motif lies directly at the docking point of COX I helix 3 and cytochrome c, and modeling of bovine COX I suggests the possibility of an unprecedented helix-terminating disulfide bridge that could alter COX/cytochrome c dissociation kinetics. Thus, the key adaptation in Utricularia likely lies in molecular energetic changes that buttressed the mechanisms responsible for the bladderworts' radical morphological evolution. Along with evidence for COX evolution underlying expansion of the anthropoid neocortex, our findings underscore that important morphological and physiological innovations must often be accompanied by specific adaptations in proteins with basic cellular functions. molecular adaptation | positive selection | cellular energetics | protein structure | developmental regulation
The terrestrial carnivorous bladderwort, Utricularia uliginosa Vahl. (Lentibulariaceae) was studi... more The terrestrial carnivorous bladderwort, Utricularia uliginosa Vahl. (Lentibulariaceae) was studied to determine the species assemblage present in traps of these plants in situ across four sites over 15 months. The immediate soil environment was also sampled to determine the fauna present, and to compare the fauna present in traps with the fauna in the environment. The soil fauna consisted of 10 taxon types, which occupied either pelagic, epibenthic or interstitial microhabitats. All were found in traps of U. uliginosa, with the main prey being interstitial taxa followed by epibenthic and occasionally pelagic taxa. Numbers of individuals of the two most abundant soil taxa (nematodes, Elaphoidella) varied independently across the four sites over the 15 months of the study, as did numbers of Elaphoidella in the traps of U. uliginosa. Numbers of nematodes in the traps of U. uliginosa showed significant differences among sites, but not differences among times. Comparison of the trap fauna with the soil fauna revealed differences in relative abundance between soil samples and trap samples for two of the three taxa examined. There was an under-representation of nematodes in the traps relative to numbers in surrounding soil. There was an over-representation of the copepod Elaphoidella in the traps of U. uliginosa relative to numbers in soil at some of the times of sampling. Acarina were equally abundant in soil and trap samples. The patterns observed for Elaphoidella and nematodes may be due to selectivity in trapping by U. uliginosa, and/or differences in digestibility of the prey. Elaphoidella individuals were found to be attracted to U. uliginosa in a behavioural experiment. This may contribute to the over-representation of Elaphoidella in the traps of U. uliginosa in the field.
In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricular... more In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula).
Abstract: The evolution of carnivorous plants has been modeled as a selective tradeoff between ph... more Abstract: The evolution of carnivorous plants has been modeled as a selective tradeoff between photosynthetic costs and benefits in nutrient-poor habitats. Although possibly applicable for pitfall and flypaper trappers, more variables may be required for active trapping systems. Bladderwort (Utricularia) suction traps react to prey stimuli with an extremely rapid release of elastic instability. Trap setting requires considerable energy to engage an active ion transport process whereby water is pumped out through the thin bladder walls to create negative internal pressure. Accordingly, empirical estimates have shown that respiratory rates in bladders are far greater than in leafy structures. Cytochrome c oxidase (COX) is a multi-subunit enzyme that catalyzes the respiratory reduction of oxygen to water and couples this reaction to translocation of protons, generating a transmembrane electrochemical gradient that is used for the synthesis of adenosine triphosphate (ATP). We have previously demonstrated that two contiguous cysteine residues in helix 3 of COX subunit I (COX I) have evolved under positive Darwinian selection. This motif, absent in = 99.9 % of databased COX I proteins from eukaryotes, Archaea, and Bacteria, lies directly at the docking point of COX I helix 3 and cytochrome c. Modeling of bovine COX I suggests the possibility that a vicinal disulfide bridge at this position could cause premature helix termination. The helix 3–4 loop makes crucial contacts with the active site of COX, and we postulate that the C–C motif might cause a conformational change that decouples (or partly decouples) electron transport from proton pumping. Such decoupling would permit bladderworts to optimize power output (which equals energy times rate) during times of need, albeit with a 20 % reduction in overall energy efficiency of the respiratory chain. A new model for the evolution of bladderwort carnivory is proposed that includes respiration as an additional tradeoff parameter.
In the carnivorous plant family Lentibulariaceae, the bladderwort lineage (Utricularia and Genlis... more In the carnivorous plant family Lentibulariaceae, the bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula). Bladderworts have a relaxed body plan that has permitted the evolution of terrestrial, epiphytic, and aquatic forms that capture prey in intricately designed suction bladders or corkscrew-shaped lobster-pot traps. In contrast, the flypaper-trapping butterworts maintain vegetative structures typical of angiosperms. We found that bladderwort genomes evolve significantly faster across seven loci (the trnL intron, the second trnL exon, the trnL–F intergenic spacer, the rps16 intron, rbcL, coxI, and 5.8S rDNA) representing all three genomic compartments. Generation time differences did not show a significant association. We relate these findings to the contested speciation rate hypothesis, which postulates a relationship between increased nucleotide substitution and increased cladogenesis.
Carnivorous plants inhabit nutrient-poor environments, where prominent targets of prey capture ar... more Carnivorous plants inhabit nutrient-poor environments, where prominent targets of prey capture are organic nitrogen and phosphorus.
In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricular... more In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula).
Phylogenetic relationships among 26 of the 37 recognised taxa of Utricularia subgenus Polypomphol... more Phylogenetic relationships among 26 of the 37 recognised taxa of Utricularia subgenus Polypompholyx sensu Müller & Borsch were assessed by cladistic analysis of DNA sequences from the plastid rps16 intron. We also examined the placement of the recently described U. simmonsii (sect. Minutae), which was reported to share some morphological characters with subgenus Polypompholyx. We found strong jackknife support for a monophyletic subgenus Polypompholyx lineage; however, our strict consensus tree shows an unresolved relationship between the sections Polypompholyx and Pleiochasia. Within the section Pleiochasia, we found two supported clades, generally differing in a more northern or southern distribution. Despite high levels of morphological heterogeneity and convergence, we found some clade-specific character homogeneity within these two clades, particularly that of growth and bladder-trap form, and floral structure. Bladder-trap form corresponds most strongly with terrestrial v. aquatic habits. The evolution of filiform corolla appendages corresponds with floral colour, and is possibly associated with sexual mimicry, with those of the upper corolla arising twice independently. Furthermore, we found that U. monanthos and U. novae-zelandiae remain synonyms of U. dichotoma, and that U. simmonsii is not included in the subgenus Polypompholyx, but instead is allied with sections Stomoisia and Enskide of subgenus Bivalvaria.
In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricular... more In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula).
Nucleotide sequences of seven chloroplast (atpB and rbcL, SSU and LSU rDNAs), mitochondrial (atp1... more Nucleotide sequences of seven chloroplast (atpB and rbcL, SSU and LSU rDNAs), mitochondrial (atp1, LSU rDNA), and nuclear (18S rDNA) genes from 192 land plants and their algal relatives were analyzed using maximum likelihood and maximum parsimony ...
Proceedings of The National Academy of Sciences, 2004
Much recent attention in the study of adaptation of organismal form has centered on developmental... more Much recent attention in the study of adaptation of organismal form has centered on developmental regulation. As such, the highly conserved respiratory machinery of eukaryotic cells might seem an unlikely target for selection supporting novel morphologies. We demonstrate that a dramatic molecular evolutionary rate increase in subunit I of cytochrome c oxidase (COX) from an active-trapping lineage of carnivorous plants is caused by positive Darwinian selection. Bladderworts (Utricularia) trap plankton when water-immersed, negatively pressured suction bladders are triggered. The resetting of traps involves active ion transport, requiring considerable energy expenditure. As judged from the quaternary structure of bovine COX, the most profound adaptive substitutions are two contiguous cysteines absent in 99.9% of databased COX I sequences from Eukaryota, Archaea, and Bacteria. This motif lies directly at the docking point of COX I helix 3 and cytochrome c, and modeling of bovine COX I suggests the possibility of an unprecedented helix-terminating disulfide bridge that could alter COX/cytochrome c dissociation kinetics. Thus, the key adaptation in Utricularia likely lies in molecular energetic changes that buttressed the mechanisms responsible for the bladderworts' radical morphological evolution. Along with evidence for COX evolution underlying expansion of the anthropoid neocortex, our findings underscore that important morphological and physiological innovations must often be accompanied by specific adaptations in proteins with basic cellular functions. molecular adaptation | positive selection | cellular energetics | protein structure | developmental regulation
The terrestrial carnivorous bladderwort, Utricularia uliginosa Vahl. (Lentibulariaceae) was studi... more The terrestrial carnivorous bladderwort, Utricularia uliginosa Vahl. (Lentibulariaceae) was studied to determine the species assemblage present in traps of these plants in situ across four sites over 15 months. The immediate soil environment was also sampled to determine the fauna present, and to compare the fauna present in traps with the fauna in the environment. The soil fauna consisted of 10 taxon types, which occupied either pelagic, epibenthic or interstitial microhabitats. All were found in traps of U. uliginosa, with the main prey being interstitial taxa followed by epibenthic and occasionally pelagic taxa. Numbers of individuals of the two most abundant soil taxa (nematodes, Elaphoidella) varied independently across the four sites over the 15 months of the study, as did numbers of Elaphoidella in the traps of U. uliginosa. Numbers of nematodes in the traps of U. uliginosa showed significant differences among sites, but not differences among times. Comparison of the trap fauna with the soil fauna revealed differences in relative abundance between soil samples and trap samples for two of the three taxa examined. There was an under-representation of nematodes in the traps relative to numbers in surrounding soil. There was an over-representation of the copepod Elaphoidella in the traps of U. uliginosa relative to numbers in soil at some of the times of sampling. Acarina were equally abundant in soil and trap samples. The patterns observed for Elaphoidella and nematodes may be due to selectivity in trapping by U. uliginosa, and/or differences in digestibility of the prey. Elaphoidella individuals were found to be attracted to U. uliginosa in a behavioural experiment. This may contribute to the over-representation of Elaphoidella in the traps of U. uliginosa in the field.
In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricular... more In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula).
Abstract: The evolution of carnivorous plants has been modeled as a selective tradeoff between ph... more Abstract: The evolution of carnivorous plants has been modeled as a selective tradeoff between photosynthetic costs and benefits in nutrient-poor habitats. Although possibly applicable for pitfall and flypaper trappers, more variables may be required for active trapping systems. Bladderwort (Utricularia) suction traps react to prey stimuli with an extremely rapid release of elastic instability. Trap setting requires considerable energy to engage an active ion transport process whereby water is pumped out through the thin bladder walls to create negative internal pressure. Accordingly, empirical estimates have shown that respiratory rates in bladders are far greater than in leafy structures. Cytochrome c oxidase (COX) is a multi-subunit enzyme that catalyzes the respiratory reduction of oxygen to water and couples this reaction to translocation of protons, generating a transmembrane electrochemical gradient that is used for the synthesis of adenosine triphosphate (ATP). We have previously demonstrated that two contiguous cysteine residues in helix 3 of COX subunit I (COX I) have evolved under positive Darwinian selection. This motif, absent in = 99.9 % of databased COX I proteins from eukaryotes, Archaea, and Bacteria, lies directly at the docking point of COX I helix 3 and cytochrome c. Modeling of bovine COX I suggests the possibility that a vicinal disulfide bridge at this position could cause premature helix termination. The helix 3–4 loop makes crucial contacts with the active site of COX, and we postulate that the C–C motif might cause a conformational change that decouples (or partly decouples) electron transport from proton pumping. Such decoupling would permit bladderworts to optimize power output (which equals energy times rate) during times of need, albeit with a 20 % reduction in overall energy efficiency of the respiratory chain. A new model for the evolution of bladderwort carnivory is proposed that includes respiration as an additional tradeoff parameter.
In the carnivorous plant family Lentibulariaceae, the bladderwort lineage (Utricularia and Genlis... more In the carnivorous plant family Lentibulariaceae, the bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula). Bladderworts have a relaxed body plan that has permitted the evolution of terrestrial, epiphytic, and aquatic forms that capture prey in intricately designed suction bladders or corkscrew-shaped lobster-pot traps. In contrast, the flypaper-trapping butterworts maintain vegetative structures typical of angiosperms. We found that bladderwort genomes evolve significantly faster across seven loci (the trnL intron, the second trnL exon, the trnL–F intergenic spacer, the rps16 intron, rbcL, coxI, and 5.8S rDNA) representing all three genomic compartments. Generation time differences did not show a significant association. We relate these findings to the contested speciation rate hypothesis, which postulates a relationship between increased nucleotide substitution and increased cladogenesis.
Carnivorous plants inhabit nutrient-poor environments, where prominent targets of prey capture ar... more Carnivorous plants inhabit nutrient-poor environments, where prominent targets of prey capture are organic nitrogen and phosphorus.
In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricular... more In the carnivorous plant family Lentibulariaceae, the INTRODUCTION bladderwort lineage (Utricularia and Genlisea) is substantially more species-rich and morphologically divergent than its sister lineage, the butterworts (Pinguicula).
Phylogenetic relationships among 26 of the 37 recognised taxa of Utricularia subgenus Polypomphol... more Phylogenetic relationships among 26 of the 37 recognised taxa of Utricularia subgenus Polypompholyx sensu Müller & Borsch were assessed by cladistic analysis of DNA sequences from the plastid rps16 intron. We also examined the placement of the recently described U. simmonsii (sect. Minutae), which was reported to share some morphological characters with subgenus Polypompholyx. We found strong jackknife support for a monophyletic subgenus Polypompholyx lineage; however, our strict consensus tree shows an unresolved relationship between the sections Polypompholyx and Pleiochasia. Within the section Pleiochasia, we found two supported clades, generally differing in a more northern or southern distribution. Despite high levels of morphological heterogeneity and convergence, we found some clade-specific character homogeneity within these two clades, particularly that of growth and bladder-trap form, and floral structure. Bladder-trap form corresponds most strongly with terrestrial v. aquatic habits. The evolution of filiform corolla appendages corresponds with floral colour, and is possibly associated with sexual mimicry, with those of the upper corolla arising twice independently. Furthermore, we found that U. monanthos and U. novae-zelandiae remain synonyms of U. dichotoma, and that U. simmonsii is not included in the subgenus Polypompholyx, but instead is allied with sections Stomoisia and Enskide of subgenus Bivalvaria.
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