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Extremely low microsatellite diversity but distinct population structure in a long-lived threatened species, the Australian lungfish Neoceratodus forsteri (Dipnoi).

Hughes JM, Schmidt DJ, Huey JA, Real KM, Espinoza T, McDougall A, Kind PK, Brooks S, Roberts DT - PLoS ONE (2015)

Bottom Line: We test whether there is significant genetic structure among and within river drainages; assign putatively translocated populations to potential source populations; and estimate effective population sizes.We were unable to obtain bounded estimates of effective population size, as we have too few genotype combinations, although point estimates were low, ranging from 29 - 129.We recommend that, in order to preserve any local adaptation in the three distinct populations that they be managed separately.

View Article: PubMed Central - PubMed

Affiliation: Australian Rivers Institute, Griffith University, Brisbane, Queensland, Australia.

ABSTRACT
The Australian lungfish is a unique living representative of an ancient dipnoan lineage, listed as 'vulnerable' to extinction under Australia's Environment Protection and Biodiversity Conservation Act 1999. Historical accounts indicate this species occurred naturally in two adjacent river systems in Australia, the Burnett and Mary. Current day populations in other rivers are thought to have arisen by translocation from these source populations. Early genetic work detected very little variation and so had limited power to answer questions relevant for management including how genetic variation is partitioned within and among sub-populations. In this study, we use newly developed microsatellite markers to examine samples from the Burnett and Mary Rivers, as well as from two populations thought to be of translocated origin, Brisbane and North Pine. We test whether there is significant genetic structure among and within river drainages; assign putatively translocated populations to potential source populations; and estimate effective population sizes. Eleven polymorphic microsatellite loci genotyped in 218 individuals gave an average within-population heterozygosity of 0.39 which is low relative to other threatened taxa and for freshwater fishes in general. Based on FST values (average over loci = 0.11) and STRUCTURE analyses, we identify three distinct populations in the natural range, one in the Burnett and two distinct populations in the Mary. These analyses also support the hypothesis that the Mary River is the likely source of translocated populations in the Brisbane and North Pine rivers, which agrees with historical published records of a translocation event giving rise to these populations. We were unable to obtain bounded estimates of effective population size, as we have too few genotype combinations, although point estimates were low, ranging from 29 - 129. We recommend that, in order to preserve any local adaptation in the three distinct populations that they be managed separately.

No MeSH data available.


Sample sites and clustering analysis of multilocus microsatellite data performed using STRUCTURE software.(A) Map of southeast Queensland highlighting sampled catchments and the seven sampling locations. (B) Plot of values for the mean likelihood of each genetic cluster (K) for K = 1 to 8, where the error bar represents one standard deviation. (C) Plot of Delta K calculated as the mean of the second-order rate of change in likelihood of K divided by the standard deviation of the likelihood of K. (D) Bar plot of estimated membership of each individual in K = 4 clusters. Black bars separate the seven population sample groups. (E) Bar plot of estimated membership of each individual in K = 5 clusters. (F) Genetic assignment of translocated population samples to three reference genetic groups (K = 3) representing three genetically distinct natural populations. Three reference groups comprise individuals from Burnett River, Mary River and Tinana Creek. Unknown groups assigned to the reference comprise individuals from North Pine River and Brisbane River.
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pone.0121858.g001: Sample sites and clustering analysis of multilocus microsatellite data performed using STRUCTURE software.(A) Map of southeast Queensland highlighting sampled catchments and the seven sampling locations. (B) Plot of values for the mean likelihood of each genetic cluster (K) for K = 1 to 8, where the error bar represents one standard deviation. (C) Plot of Delta K calculated as the mean of the second-order rate of change in likelihood of K divided by the standard deviation of the likelihood of K. (D) Bar plot of estimated membership of each individual in K = 4 clusters. Black bars separate the seven population sample groups. (E) Bar plot of estimated membership of each individual in K = 5 clusters. (F) Genetic assignment of translocated population samples to three reference genetic groups (K = 3) representing three genetically distinct natural populations. Three reference groups comprise individuals from Burnett River, Mary River and Tinana Creek. Unknown groups assigned to the reference comprise individuals from North Pine River and Brisbane River.

Mentions: The Australian lungfish Neoceratodus forsteri is the most primitive member of the subclass Dipnoi, and the only extant representative of the group in Australia [9]. Australian lungfish reach large sizes (up to 150 cm and 20 kg) and are very long-lived, with some individuals known to live for over 80 years [9,10]. The species also has a very long evolutionary history, having existed with little change in morphology for around 100 million years since the early Cretaceous [9,11]. The Australian lungfish was historically widespread in drainages of eastern Australia before its range contracted to a small area of southeastern Queenlsand during the Pleistocene [12]. The species is currently only found in a few rivers in southeast Queensland, although it is thought to occur naturally in only two river systems, the Mary River and the Burnett River [9,13] see Fig 1A. Populations in other rivers (Brisbane, North Pine, Condamine, Coomera, Albert, see Fig 1A), are thought to be the result of translocations, some of which were documented in the late nineteenth century [14]. Recruitment of juveniles into the population has rarely been observed since the discovery of the lungfish in 1870, leading to the belief that the population may be at risk of extinction [15] and that translocation was an option to increase the distribution and spread the risk across multiple river systems [16]. Lungfish are quite abundant in parts of the Brisbane River (David Roberts, pers comm.), with fewer in the North Pine River and fewer individuals in the other rivers to which they were translocated. Populations are all dominated by adults, with little evidence of recent or regular recruitment in most of these populations [17]. It has been declared a nationally vulnerable species under the Environment Protection and Biodiversity Conservation Act 1999 and is listed as a no-take species under Schedule 2 of the Fisheries Regulation 2008 under the Fisheries Act 1999 (Queensland). For the purposes of managing lungfish populations, Fisheries Queensland has always assumed that Burnett and Mary populations are natural and that the other populations have resulted from translocation (Peter Kind, pers comm.).


Extremely low microsatellite diversity but distinct population structure in a long-lived threatened species, the Australian lungfish Neoceratodus forsteri (Dipnoi).

Hughes JM, Schmidt DJ, Huey JA, Real KM, Espinoza T, McDougall A, Kind PK, Brooks S, Roberts DT - PLoS ONE (2015)

Sample sites and clustering analysis of multilocus microsatellite data performed using STRUCTURE software.(A) Map of southeast Queensland highlighting sampled catchments and the seven sampling locations. (B) Plot of values for the mean likelihood of each genetic cluster (K) for K = 1 to 8, where the error bar represents one standard deviation. (C) Plot of Delta K calculated as the mean of the second-order rate of change in likelihood of K divided by the standard deviation of the likelihood of K. (D) Bar plot of estimated membership of each individual in K = 4 clusters. Black bars separate the seven population sample groups. (E) Bar plot of estimated membership of each individual in K = 5 clusters. (F) Genetic assignment of translocated population samples to three reference genetic groups (K = 3) representing three genetically distinct natural populations. Three reference groups comprise individuals from Burnett River, Mary River and Tinana Creek. Unknown groups assigned to the reference comprise individuals from North Pine River and Brisbane River.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390199&req=5

pone.0121858.g001: Sample sites and clustering analysis of multilocus microsatellite data performed using STRUCTURE software.(A) Map of southeast Queensland highlighting sampled catchments and the seven sampling locations. (B) Plot of values for the mean likelihood of each genetic cluster (K) for K = 1 to 8, where the error bar represents one standard deviation. (C) Plot of Delta K calculated as the mean of the second-order rate of change in likelihood of K divided by the standard deviation of the likelihood of K. (D) Bar plot of estimated membership of each individual in K = 4 clusters. Black bars separate the seven population sample groups. (E) Bar plot of estimated membership of each individual in K = 5 clusters. (F) Genetic assignment of translocated population samples to three reference genetic groups (K = 3) representing three genetically distinct natural populations. Three reference groups comprise individuals from Burnett River, Mary River and Tinana Creek. Unknown groups assigned to the reference comprise individuals from North Pine River and Brisbane River.
Mentions: The Australian lungfish Neoceratodus forsteri is the most primitive member of the subclass Dipnoi, and the only extant representative of the group in Australia [9]. Australian lungfish reach large sizes (up to 150 cm and 20 kg) and are very long-lived, with some individuals known to live for over 80 years [9,10]. The species also has a very long evolutionary history, having existed with little change in morphology for around 100 million years since the early Cretaceous [9,11]. The Australian lungfish was historically widespread in drainages of eastern Australia before its range contracted to a small area of southeastern Queenlsand during the Pleistocene [12]. The species is currently only found in a few rivers in southeast Queensland, although it is thought to occur naturally in only two river systems, the Mary River and the Burnett River [9,13] see Fig 1A. Populations in other rivers (Brisbane, North Pine, Condamine, Coomera, Albert, see Fig 1A), are thought to be the result of translocations, some of which were documented in the late nineteenth century [14]. Recruitment of juveniles into the population has rarely been observed since the discovery of the lungfish in 1870, leading to the belief that the population may be at risk of extinction [15] and that translocation was an option to increase the distribution and spread the risk across multiple river systems [16]. Lungfish are quite abundant in parts of the Brisbane River (David Roberts, pers comm.), with fewer in the North Pine River and fewer individuals in the other rivers to which they were translocated. Populations are all dominated by adults, with little evidence of recent or regular recruitment in most of these populations [17]. It has been declared a nationally vulnerable species under the Environment Protection and Biodiversity Conservation Act 1999 and is listed as a no-take species under Schedule 2 of the Fisheries Regulation 2008 under the Fisheries Act 1999 (Queensland). For the purposes of managing lungfish populations, Fisheries Queensland has always assumed that Burnett and Mary populations are natural and that the other populations have resulted from translocation (Peter Kind, pers comm.).

Bottom Line: We test whether there is significant genetic structure among and within river drainages; assign putatively translocated populations to potential source populations; and estimate effective population sizes.We were unable to obtain bounded estimates of effective population size, as we have too few genotype combinations, although point estimates were low, ranging from 29 - 129.We recommend that, in order to preserve any local adaptation in the three distinct populations that they be managed separately.

View Article: PubMed Central - PubMed

Affiliation: Australian Rivers Institute, Griffith University, Brisbane, Queensland, Australia.

ABSTRACT
The Australian lungfish is a unique living representative of an ancient dipnoan lineage, listed as 'vulnerable' to extinction under Australia's Environment Protection and Biodiversity Conservation Act 1999. Historical accounts indicate this species occurred naturally in two adjacent river systems in Australia, the Burnett and Mary. Current day populations in other rivers are thought to have arisen by translocation from these source populations. Early genetic work detected very little variation and so had limited power to answer questions relevant for management including how genetic variation is partitioned within and among sub-populations. In this study, we use newly developed microsatellite markers to examine samples from the Burnett and Mary Rivers, as well as from two populations thought to be of translocated origin, Brisbane and North Pine. We test whether there is significant genetic structure among and within river drainages; assign putatively translocated populations to potential source populations; and estimate effective population sizes. Eleven polymorphic microsatellite loci genotyped in 218 individuals gave an average within-population heterozygosity of 0.39 which is low relative to other threatened taxa and for freshwater fishes in general. Based on FST values (average over loci = 0.11) and STRUCTURE analyses, we identify three distinct populations in the natural range, one in the Burnett and two distinct populations in the Mary. These analyses also support the hypothesis that the Mary River is the likely source of translocated populations in the Brisbane and North Pine rivers, which agrees with historical published records of a translocation event giving rise to these populations. We were unable to obtain bounded estimates of effective population size, as we have too few genotype combinations, although point estimates were low, ranging from 29 - 129. We recommend that, in order to preserve any local adaptation in the three distinct populations that they be managed separately.

No MeSH data available.