Genetic diversity of coastal bottlenose dolphins revealed by structurally and functionally diverse hemoglobins

Abstract

Studies of structure-function relationships in the respiratory proteins of marine mammals revealed unexpected variations in the number and types of hemoglobins (Hbs) present in coastal bottlenose dolphins, Tursiops truncatus. We obtained blood samples from free-ranging coastal bottlenose dolphins as a component of capture-release studies. We found that the oxygen-binding functions of bottlenose dolphin blood are poised between effector-saturated and unsaturated levels, enabling exercise-dependent shifts in oxygen transfer functions. Isolated bottlenose dolphin Hbs showed elevated pH sensitivities (Bohr effects) and appreciably lower oxygen affinities than adult human Hb in the absence of allosteric effectors. These properties may be an adaptive modification that enhance oxygen delivery during diving episodes when oxygen tensions and effector levels are low. The Hbs of individual dolphins showed similar oxygen affinities, responses to effectors, and expression of heme-heme interaction in oxygen binding, but differed in their redox potentials and rates of autoxidation. The heterogeneity suggested by these functional variations in Hbs of individual dolphins was born out by variations in the molecular weights and numbers of their α and β globin chains. Although coastal bottlenose dolphins were expected to have a single type of Hb, the mass differences observed revealed considerable genetic diversity. There were multiple Hb forms in some individuals and differences in Hb patterns among individuals within the same community.Keywords population diverstiy; alleles; oxygen binding; allostery; redox chemistry *Address correspondence to: Celia Bonaventura, Duke University Marine Laboratory, Beaufort, NC 28516, Tel. 252−505−7591; Fax 252−728−6824, E-Mail: bona@duke.edu.. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. IntroductionBottlenose dolphins are widely distributed in both coastal and offshore waters throughout the world. Their relatively easy accessibility by researchers has made them one of the most frequently studied marine mammals (Leatherwood and Reeves, 1990). Despite this, few studies have sought to describe the characteristics of bottlenose dolphin hemoglobin (Hb). Our studies add to knowledge of these diving mammals by documenting exercise-dependent oxygenbinding functions of whole blood, by determining oxygen binding and oxidative functions of bottlenose dolphin Hb in the presence and absence of allosteric effectors, and by showing an unexpected diversity in coastal bottlenose dolphins Hbs.Hb is found in the erythrocytes of dolphins and other vertebrates and...

Heme proteins and oxidation in fresh and processed meats

“…A sampling of 27 coastal bottlenose dolphins (Turiops truncatus) exhibited different Hb oxidation rates (Remington et al, 2007). This was attributed to the observation that some dolphins had Hb isoforms that differed compared to the other dolphins examined.…”

Genomic Organization and Differential Signature of Positive Selection in the Alpha and Beta Globin Gene Clusters in Two Cetacean Species

“…Although a few cetacean α- and β-globins have been sequenced so far and analyzed functionally ( Brix et al 1990 ; Tellone et al 2000 ; Corda et al 2003 ; Remington et al 2007 ; Manconi et al 2009 ), no previous work has characterized the α- and β-globins clusters on this particular lineage. Most of the earlier studies have shown that the oxygen-binding behavior of cetaceans’ hemoglobin has unusual properties probably linked to their peculiar diving behavior: lower intrinsic oxygen affinities and greater Bohr effects.…”

“…These characteristics could enhance oxygen release to respiring tissues when exercise causes a drop in levels of ATP. Remington et al (2007) highlighted that the relative low-oxygen affinities are intrinsic to the Hb’s structure and showed that genetic diversity was clearly responsible for the variations in Hb type and function of these animals.…”

Phylogeography, genetic diversity and population structure of common bottlenose dolphins in the Wider Caribbean inferred from analyses of mitochondrial DNA control region sequences and microsatellite loci: conservation and management implications

“…Despite the potential for long‐distance dispersal within T. truncatus , significant population structure over relatively small geographic distances have been detected among coastal regional populations such as those found along the coasts of the Gulf of Mexico, Florida, Bahamas, New Zealand, United Kingdom, Mediterranean and Black Seas (Wells, ; Hoelzel et al ., ; Parsons et al ., ; Torres et al ., ; Natoli et al ., , ; Sellas et al ., ; Parsons et al ., ; Remington et al ., ; Viaud‐Martínez et al ., ; Tezanos‐Pinto et al ., ; Urian et al ., ). The only T. truncatus population studied to date, where no significant population structure was found is in the North Atlantic off the Azores and Madeira (Quérouil et al ., ).…”