Genome-wide association study of an unusual dolphin mortality event reveals candidate genes for susceptibility and resistance to cetacean morbillivirus

Infectious diseases are significant demographic and evolutionary drivers of populations, but studies about the genetic basis of disease resistance and susceptibility are scarce in wildlife populations. Cetacean morbillivirus (CeMV) is a highly contagious disease that is increasing in both geographic distribution and incidence, causing unusual mortality events (UME) and killing tens of thousands of individuals across multiple cetacean species worldwide since the late 1980s. The largest CeMV outbreak in the Southern Hemisphere reported to date occurred in Australia in 2013, where it was a major factor in a UME, killing mainly young Indo-Pacific bottlenose dolphins (Tursiops aduncus). Using cases (nonsurvivors) and controls (putative survivors) from the most affected population, we carried out a genome-wide association study to identify candidate genes for resistance and susceptibility to CeMV. The genomic data set consisted of 278,147,988 sequence reads and 35,493 high-quality SNPs genotyped across 38 individuals. Association analyses found highly significant differences in allele and genotype frequencies among cases and controls at 65 SNPs, and Random Forests conservatively identified eight as candidates. Annotation of these SNPs identified five candidate genes (MAPK8, FBXW11, INADL, ANK3 and ACOX3) with functions associated with stress, pain and immune responses. Our findings provide the first insights into the genetic basis of host defence to this highly contagious disease, enabling the development of an applied evolutionary framework to monitor CeMV resistance across cetacean species. Biomarkers could now be established to assess potential risk factors associated with these genes in other CeMV-affected cetacean populations and species. These results could also possibly aid in the advancement of vaccines against morbilliviruses.Kimberley C. Batley, Jonathan Sandoval‐Castillo, Catherine M. Kemper, Catherine R. M. Attard, Nikki Zanardo, Ikuko Tomo, Luciano B. Beheregaray, Luciana M. Mölle

Population connectivity of the highly migratory shortfin mako (Isurus oxyrinchus Rafinesque 1810) and implications for management in the Southern Hemisphere

Published: 20 November 2018In this paper we combine analyses of satellite telemetry and molecular data to investigate spatial connectivity and genetic structure among populations of shortfin mako (Isurus oxyrinchus) in and around Australian waters, where this species is taken in recreational and commercial fisheries. Mitochondrial DNA data suggest matrilineal substructure across hemispheres, while nuclear DNA data indicate shortfin mako may constitute a globally panmictic population. There was generally high genetic connectivity within Australian waters. Assessing genetic connectivity across the Indian Ocean basin, as well as the extent that shortfin mako exhibit sex biases in dispersal patterns would benefit from future improved sampling of adult size classes, particularly of individuals from the eastern Indian Ocean. Telemetry data indicated that Australasian mako are indeed highly migratory and frequently make long-distance movements. However, individuals also exhibit fidelity to relatively small geographic areas for extended periods. Together these patterns suggest that shortfin mako populations may be genetically homogenous across large geographical areas as a consequence of few reproductively active migrants, although spatial partitioning exists. Given that connectivity appears to occur at different scales, management at both the national and regional levels seems most appropriate.Shannon Corrigan, Andrew D. Lowther, Luciano B. Beheregaray, Barry D. Bruce, Geremy Cliff, Clinton A. Duffy, Alan Foulis, Malcolm P. Francis, Simon D. Goldsworthy, John R. Hyde, Rima W. Jabado, Dovi Kacev, Lindsay Marshall, Gonzalo R. Mucientes, Gavin J. P. Naylor, Julian G. Pepperell, Nuno Queiroz, William T. White, Sabine P. Wintner and Paul J. Roger

Permanent Genetic Resources added to Molecular Ecology Resources Database 1 February 2013-31 March 2013

This article documents the addition of 142 microsatellite marker loci to the Molecular Ecology Resources database. Loci were developed for the following species: Agriophyllum squarrosum, Amazilia cyanocephala, Batillaria attramentaria, Fungal strain CTeY1 (Ascomycota), Gadopsis marmoratus, Juniperus phoenicea subsp. turbinata, Liriomyza sativae, Lupinus polyphyllus, Metschnikowia reukaufii, Puccinia striiformis and Xylocopa grisescens. These loci were cross-tested on the following species: Amazilia beryllina, Amazilia candida, Amazilia rutila, Amazilia tzacatl, Amazilia violiceps, Amazilia yucatanensis, Campylopterus curvipennis, Cynanthus sordidus, Hylocharis leucotis, Juniperus brevifolia, Juniperus cedrus, Juniperus osteosperma, Juniperus oxycedrus, Juniperus thurifera, Liriomyza bryoniae, Liriomyza chinensis, Liriomyza huidobrensis and Liriomyza trifolii. © 2013 John Wiley & Sons Ltd.Peer Reviewe

Environmental and social influences on the genetic structure of bottlenose dolphins (Tursiops aduncus) in Southeastern Australia

Determining genetic connectivity of bottlenose dolphin communities helps identify evolutionary mechanisms, such as environmental and social factors, that interact to shape dispersal in highly social marine mammals. Here, we expand on a localized study that found marked genetic differentiation among resident dolphins (Tursiops aduncus) in the Port Stephens embayment and adjacent coastal communities, to include four additional communities inhabiting different environment types along the New South Wales coast, Southeastern Australia. Analysis of the mitochondrial DNA control region and seven microsatellite loci suggest the nine communities may have originated from a single ancestral population that progressively colonised the coast in a southward direction. Gene flow among communities was predominately governed by habitat type. The two enclosed embayments showed the highest level of genetic differentiation from other communities, while genetic differentiation among coastal and open embayment communities generally followed a pattern of isolation by distance. Directional bias in recent migration rates was evident, with the centrally located Hunter coast communities consisting of individuals with mixed ancestry from the Northern, Southern and Port Stephens communities. Emigration from Port Stephens was substantially higher than in the opposite direction, indicating there may be social barriers to dispersal created by Port Stephens dolphins. Our results suggest that the scale of connectivity of bottlenose dolphin communities inhabiting heterogeneous environments is likely to be affected by local habitat adaptation. This has important implications for the management of communities exposed to increasing levels of anthropogenic disturbances, such as the intensive commercial dolphin-watching industry operating in Port Stephens

Environmental influences on the genetic structure of Indo-Pacific bottlenose dolphins (Tursiops aduncus) in southeastern Australia

Determining genetic connectivity of bottlenose dolphin communities facilitates the identification of environmental and social factors that interact to shape dispersal in highly social marine mammals. Here, we examine the genetic structure and dispersal patterns among nine bottlenose dolphin (Tursiops aduncus) communities inhabiting different environment types (embayment and open coast) along the New South Wales coast from Eden to Byron Bay. Analysis of the mitochondrial DNA control region and seven microsatellite loci suggested the nine communities originated from a single ancestral population that progressively colonised the coast in a southward direction. Contemporary gene flow among communities, however, was predominately governed by habitat type. The two enclosed embayments (Port Stephens and Yamba) showed highest levels of genetic differentiation to dolphin communities ranging on the coast or in open embayments. Genetic differentiation among these coastal and open embayment communities generally followed a pattern of isolation by distance. Directional bias in recent migration rates was evident, with the centrally located Hunter communities consisting of individuals with mixed ancestry from the Northern NSW, Southern NSW and Port Stephens communities. Emigration from Port Stephens was substantially higher than in the opposite direction, indicating there may be social barriers to dispersal created by resident Port Stephens dolphins. Our results suggest that the scale of connectivity of bottlenose dolphins inhabiting heterogeneous environments is affected by local habitat adaptation. This has important implications to the management of communities exposed to increasing levels of anthropogenic disturbances, such as the intensive commercial dolphin-watching industry operating in Port Stephens

Habitat type promotes rapid and extremely localised genetic differentiation in dolphins

The high potential for dispersal of many marine organisms often results in low population differentiation over large distances. Here, we report that dolphin communities living in very close geographic proximity (<16 km) but in two different environments – open coast and enclosed embayment – exhibit unexpected genetic differentiation at nine microsatellite loci. Results based on a fixation index and a Bayesian clustering approach suggested that gene flow between communities within an embayment is high, as is gene flow between coastal communities. However, lower gene flow between embayment and open coast communities translated into substantial genetic differentiation between dolphin communities from the two environments, and assignment of individuals into two populations. Along with patterns observed in 403 bp of the mitochondrial DNA control region, the results suggest that restriction of gene flow likely occurred in the last 6000 years, after coastal dolphins colonised the embayment. We hypothesise that factors such as fidelity to the local area and resource and behavioural specialisations may have played a major role in promoting and maintaining genetic subdivision between dolphins of the two environments. Importantly, our study shows that habitat type can rapidly promote extremely fine-scale genetic structure in a long-lived, highly mobile marine mammal

SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology

All genetic markers are estimators of DNA nucleotide sequence variation. Rather than obtaining DNA sequence data, it is cheaper and faster to use techniques that estimate sequence variation, although this usually results in the loss of some information. SSCP (single-stranded conformation polymorphism) offers a sensitive but inexpensive, rapid, and convenient method for determining which DNA samples in a set differ in sequence, so that only an informative subset need be sequenced. In short, most DNA sequence variation can be detected with relatively little sequencing. SSCP has been widely applied in medical diagnosis, yet few studies have been published in population genetics. The utility and convenience of SSCP is far from fully appreciated by molecular population biologists. We hope to help redress this by illustrating the application of a single simple SSCP protocol to mitochondrial genes, nuclear introns, microsatellites, and anonymous nuclear sequences, in a range of vertebrates and invertebrates

Fine-scale genetic structure in short-beaked common dolphins (Delphinus delphis) along the East Australian Current

Oceanographic processes play a significant role in shaping the genetic structure of marine populations, but it is less clear whether they affect genetic differentiation of highly mobile vertebrates. We used microsatellite markers and mtDNA control region sequences to investigate the spatial genetic structure of short-beaked common dolphins (Delphinus delphis) in southeastern Australia, a region characterised by complex oceanographic conditions associated with the East Australian Current (EAC). A total of 115 biopsy samples of dolphins were collected from six localities spanning approximately 1,000 km of the New South Wales (NSW) coastline. We found evidence for contrasting genetic diversity and fine-scale genetic structure, characterised by three genetically differentiated populations with varying levels of admixture. Spatial genetic structure was not explained by a model of isolation by distance, instead it coincides with main patterns of oceanographic variation along the EAC. We propose that common dolphins along the EAC may be adapted to three water masses recently characterised in this region

A hybrid zone and bidirectional introgression between two catadromous species: Australian bass Macquaria novemaculeata and estuary perch Macquaria colonorum

The presence and distribution of hybrid individuals and the existence of a hybrid zone between the catadromous Australian bass Macquaria novemaculeata and estuary perch Macquaria colonorum were investigated throughout the range of both species in Australia. Bayesian analyses and genotypic simulations identified 140 putative hybrids (11.5% of the total sample) with varying levels of introgression. Most hybrids were observed in an area extending from the Snowy River to the Albert River suggesting a hybrid zone in the eastern Bass Strait region. Sixteen hybrids, however, were found outside this zone, possibly reflecting the movement of hybrid offspring between estuaries or their inadvertent release during fish stocking programmes. Biparental backcrossing was found to occur suggesting that hybrids were fertile. These results have implications for the management of the extensive stocking programme in M. novemaculeata and for understanding the potential role of habitat degradation and reduced water flow in facilitating hybridization in species with migratory life histories