Parentage Assignment Reveals Multiple Paternity in the Critically-Endangered Guatemalan Beaded Lizard (Heloderma Charlesbogerti)

Abstract Within captive management programs for species of conservation concern, understanding the genetic mating system is of fundamental importance, given its role in generating and maintaining genetic diversity and promoting opportunities for sperm competition. If a goal of a conservation program is reintroduction, knowledge of the mating system may also inform prediction models aimed at understanding how genetic diversity may be spatially organized, thus informing decisions regarding where and which individuals should be released in order to maximize genetic diversity in the wild population. Within captive populations, such information may also influence how animals are maintained in order to promote natural behaviors. Here we investigate the genetic mating system of the Guatemalan beaded lizard, Heloderma charlesbogerti, a member of a genus lacking such information. A group of adult male and female H. charlesbogerti were co-habited for five years during the species perceived breeding season. Through genomic parentage analysis, 50% of clutches comprising multiple offspring were found to result from polyandry, with up to three males siring offspring within single clutches. Furthermore, males were found to be polygamous both within and across seasons, and females would exhibit promiscuity across seasons. As such, within this captive environment, where opportunities existed for mating with multiple sexual partners, the genetic mating system was found to be highly promiscuous, with multiple paternity common within clutches. These findings are novel for the family Helodermatidae, and the results have broader implications about how reproductive opportunities should be managed within captive conservation programs.

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High incidence of multiple paternity in an Australian snapping turtle (Elseya albagula)

Australian Journal of Zoology ◽

10.1071/zo13009 ◽

2012 ◽

Vol 60 (6) ◽

pp. 412 ◽

Cited By ~ 3

Author(s):

Erica V. Todd ◽

David Blair ◽

Colin J. Limpus ◽

Duncan J. Limpus ◽

Dean R. Jerry

Keyword(s):

Mating System ◽

Southern Hemisphere ◽

Multiple Paternity ◽

Freshwater Turtle ◽

Snapping Turtle ◽

Species Of Conservation Concern ◽

The Family ◽

High Incidence ◽

Polymorphic Microsatellite ◽

Conservation Concern

Genetic parentage studies can provide detailed insights into the mating system dynamics of wild populations, including the prevalence and patterns of multiple paternity. Multiple paternity is assumed to be common among turtles, though its prevalence varies widely between species and populations. Several important groups remain to be investigated, including the family Chelidae, which dominate the freshwater turtle fauna of the Southern Hemisphere. We used seven polymorphic microsatellite markers to investigate the presence of multiple fathers within clutches from the white-throated snapping turtle (Elseya albagula), an Australian species of conservation concern. We uncovered a high incidence of multiple paternity, with 83% of clutches showing evidence of multiple fathers and up to three males contributing to single clutches. We confirm a largely promiscuous mating system for this species in the Burnett River, Queensland, although a lone incidence of single paternity indicates it is not the only strategy employed. These data provide the first example of multiple paternity in the Chelidae and extend our knowledge of the taxonomic breadth of multiple paternity in turtles of the Southern Hemisphere.

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Genetic mating system of the brown smoothhound shark (Mustelus henlei), including a literature review of multiple paternity in other elasmobranch species

Marine Biology ◽

10.1007/s00227-011-1851-z ◽

2011 ◽

Vol 159 (4) ◽

pp. 749-756 ◽

Cited By ~ 36

Author(s):

Rosemary J. Byrne ◽

John C. Avise

Keyword(s):

Literature Review ◽

Mating System ◽

Multiple Paternity ◽

Elasmobranch Species ◽

Genetic Mating System ◽

Mustelus Henlei

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Loss of Predator Discrimination by Critically Endangered Vancouver Island Marmots Within Five Generations of Breeding for Release

Frontiers in Conservation Science ◽

10.3389/fcosc.2021.718562 ◽

2021 ◽

Vol 2 ◽

Author(s):

Graham P. Dixon-MacCallum ◽

Johnathan L. Rich ◽

Natasha Lloyd ◽

Daniel T. Blumstein ◽

Axel Moehrenschlager

Keyword(s):

Vancouver Island ◽

Predator Recognition ◽

Critically Endangered ◽

Species Of Conservation Concern ◽

Mammalian Predators ◽

In Captivity ◽

Two Generations ◽

In The Wild ◽

Conservation Concern ◽

Changes Over Time

Conservation translocations, which involve the intentional movement and release of organisms for conservation benefit, are increasingly required to recover species of conservation concern. In order to maximize post-release survival, and to accomplish conservation translocation objectives, animals must exhibit behaviors that facilitate survival in the wild. The Vancouver Island marmot (Marmota vancouverensis) is a critically endangered endemic in Canada which has been captive-bred for 24 years for reintroductions and reinforcements that have increased the wild population from ~30 to more than 200 individuals. Despite this success many marmots are killed by predators after release and predation represents a major hurdle to full marmot recovery. To better understand if captive-bred marmots are prepared for the novel environment into which they will be released, and to determine whether such suitability changes over time, we presented taxidermy mounts of mammalian predators and non-predators to marmots that were wild-caught, and captive born for between one and five generations. We also examined mortality of offspring from marmots we tested that had been released to the wild. A minimum of 43% of offspring were killed by predators in the wild over 17 years, most by cougars. Marmots in captivity generally responded to taxidermy mounts by decreasing foraging and increasing vigilance, and overall responded more strongly to predators than non-predators, especially wolves. However, marmots in captivity for more than two generations lacked discrimination between cougars, non-predators, and controls, suggesting a rapid loss of predator recognition. This study was only possible because predator-recognition trials were initiated early in the conservation translocation program, and could then be repeated after a number of generations. The finding that changes occurred relatively rapidly (within five generations during which changes in genetic diversity were negligible) suggests that behavioral suitability may deteriorate more rapidly than genetics would suggest. Strategies addressing potential behavior loss should be considered, including sourcing additional wild individuals or pre-release training of captive-born individuals. Subsequently, post-release survival should be monitored to determine the efficacy of behavior-optimization strategies.

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The genetic mating system of the long-nosed potoroo (Potorous tridactylus) with notes on male strategies for securing paternity

Australian Journal of Zoology ◽

10.1071/zo12064 ◽

2012 ◽

Vol 60 (4) ◽

pp. 225 ◽

Cited By ~ 3

Author(s):

Greta J. Frankham ◽

Robert L. Reed ◽

Mark D. B. Eldridge ◽

Kathrine A. Handasyde

Keyword(s):

Mating System ◽

Mating Systems ◽

The Other ◽

Tissue Samples ◽

Multiple Partners ◽

Direct Competition ◽

In The Wild ◽

Genetic Mating System ◽

Potorous Tridactylus

The potoroids are a small group of cryptic macropodoid marsupials that are difficult to directly monitor in the wild. Consequently, information regarding their social and mating systems is limited. A population of long-nosed potoroos (Potorous tridactylus) on French Island, Victoria, was monitored from June 2005 to August 2010. Tissue samples were collected from 32 (19 ♂, 13 ♀) independent potoroos and 17 pouch young. We aimed to determine the genetic mating system and identify patterns of paternity through genotyping individuals at 10 microsatellite loci. Additionally, we investigated the importance of body mass and site residency as strategies in securing paternity. Twelve of the 17 pouch young sampled were assigned paternity with confidence to five males. Multiple pouch young were sampled from two long-term resident females, one of which had 10 pouch young sired by multiple partners, with some repeat paternity, while the other had three young sired by one male, suggesting that the mating system is not entirely promiscuous. Sires were recorded on site for significantly longer periods than non-sires but were not significantly larger than non-sires at conception. This suggests that sires employ strategies other than direct competition, such as scramble competition, to secure paternity in P. tridactylus.

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Multiple paternity and precocial breeding in wild Tasmanian devils, Sarcophilus harrisii (Marsupialia: Dasyuridae)

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz072 ◽

2019 ◽

Vol 128 (1) ◽

pp. 201-210 ◽

Cited By ~ 1

Author(s):

Tracey Russell ◽

Amanda Lane ◽

Judy Clarke ◽

Carolyn Hogg ◽

Katrina Morris ◽

...

Keyword(s):

Genetic Diversity ◽

Multiple Paternity ◽

First Record ◽

Good Genes ◽

Tasmanian Devil ◽

Histocompatibility Complex ◽

Insurance Programme ◽

In The Wild ◽

Marsupial Species ◽

Sarcophilus Harrisii

Abstract Polyandry, a common reproductive strategy in various animal species, has potential female benefits, which include enhanced offspring fitness. Benefits can be direct, such as reduced risk of male infanticide of offspring, or indirect, such as increased genetic diversity of offspring and the acquisition of ‘good genes’. Multiple paternity of litters has been recorded in numerous marsupial species but has not been reported in Tasmanian devils, Sarcophilus harrisii (Boitard). We investigated whether multiple paternity occurred in litters within a wild population of Tasmanian devils. Using major histocompatibility complex-linked and neutral microsatellite markers, the paternity of nine litters was analysed. We found multiple paternity in four out of nine litters and that yearling (> 1, < 2 years old) male devils were siring offspring. This is the first record of multiple paternity and of male precocial breeding in wild Tasmanian devils. To date, there are no data relating to the subsequent survival of devils from single- vs. multiple-sired litters; therefore, we do not know whether multiple paternity increases offspring survival in the wild. These results have implications for the Tasmanian devil captive insurance programme, because group housing can lead to multiple-sired litters, making the maintenance of genetic diversity over time difficult to manage.

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Very low rate of multiple paternity detected in clutches of a wild agamid lizard

Australian Journal of Zoology ◽

10.1071/zo18006 ◽

2017 ◽

Vol 65 (5) ◽

pp. 328 ◽

Cited By ~ 5

Author(s):

Jessica Hacking ◽

Devi Stuart-Fox ◽

Michael Gardner

Keyword(s):

Mating System ◽

Mating Systems ◽

Multiple Mating ◽

Multiple Paternity ◽

Squamate Reptiles ◽

Monogamous Species ◽

Male Territoriality ◽

Socially Monogamous ◽

Genetic Mating System ◽

Low Rate

Genetic mating systems described for squamate reptiles range from primarily monogamous to completely polygynandrous. The presence of female multiple mating is almost ubiquitous among squamates and even occurs, albeit at a low rate, in socially monogamous species. Here we examine the genetic mating system of the territorial tawny dragon lizard (Ctenophorus decresii). Paternity was assigned to captive-born hatchlings using eight microsatellite loci, revealing a 4% rate of multiple paternity. One-quarter of males sired more than one clutch, although multiple mating by males is likely underestimated. The rate of multiple paternity in C. decresii represents one of the lowest among squamates and may be a result of successful male territoriality. However, the observed low rate of multiple paternity does not eliminate the possibility of widespread female multiple mating due to the potential for sperm storage and sperm competition. We conclude that the tawny dragon lizard employs a predominantly polygynous genetic mating system.

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Experimental removal of introduced slider turtles offers new insight into competition with a native, threatened turtle

PeerJ ◽

10.7717/peerj.7444 ◽

2019 ◽

Vol 7 ◽

pp. e7444 ◽

Cited By ~ 2

Author(s):

Max R. Lambert ◽

Jennifer M. McKenzie ◽

Robyn M. Screen ◽

Adam G. Clause ◽

Benjamin B. Johnson ◽

...

Keyword(s):

Native Species ◽

Field Experiments ◽

Slider Turtle ◽

Species Of Conservation Concern ◽

Ecological Resources ◽

Mesocosm Experiments ◽

In The Wild ◽

Western Pond Turtle ◽

Negative Impacts ◽

Conservation Concern

The red-eared slider turtle (Trachemys scripta elegans; RES) is often considered one of the world’s most invasive species. Results from laboratory and mesocosm experiments suggest that introduced RES outcompete native turtles for key ecological resources, but such experiments can overestimate the strength of competition. We report on the first field experiment with a wild turtle community, involving introduced RES and a declining native species of conservation concern, the western pond turtle (Emys marmorata; WPT). Using a before/after experimental design, we show that after removing most of an introduced RES population, the remaining RES dramatically shifted their spatial basking distribution in a manner consistent with strong intraspecific competition. WPT also altered their spatial basking distribution after the RES removal, but in ways inconsistent with strong interspecific competition. However, we documented reduced levels of WPT basking post-removal, which may reflect a behavioral shift attributable to the lower density of the turtle community. WPT body condition also increased after we removed RES, consistent with either indirect or direct competition between WPT and RES and providing the first evidence that RES can compete with a native turtle in the wild. We conclude that the negative impacts on WPT basking by RES in natural contexts are more limited than suggested by experiments with captive turtles, although wild WPT do appear to compete for food with introduced RES. Our results highlight the importance of manipulative field experiments when studying biological invasions, and the potential value of RES removal as a management strategy for WPT.

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No correlation between neonatal fitness and heterozygosity in a reintroduced population of Père David’s deer

Current Zoology ◽

10.1093/czoolo/59.2.249 ◽

2013 ◽

Vol 59 (2) ◽

pp. 249-256 ◽

Cited By ~ 4

Author(s):

Yan Zeng ◽

Chunwang Li ◽

Linyuan Zhang ◽

Zhenyu Zhong ◽

Zhigang Jiang

Keyword(s):

Birth Weight ◽

Neonatal Mortality ◽

Microsatellite Loci ◽

Mammal Species ◽

Species Of Conservation Concern ◽

In Captivity ◽

In The Wild ◽

Père David’S Deer ◽

Genetic Bottlenecks ◽

Conservation Concern

Abstract Considering the severe impacts of genetic bottlenecks and small numbers of founders in populations of reintroduced animals, it is necessary to study inbreeding and its effect on fitness in species of conservation concern. Père David’s deer is one of few large mammal species extinct in the wild but safely preserved in captivity. Its specific background gives us the opportunity to study the relationships between heterozygosity and neonatal fitness in relocated populations. We employed five microsatellite loci to explore heterozygosity-fitness correlations in a population of Père David’s deer at the Beijing Milu Ecological Research Center. We observed associations between microsatellite-based variables sMLH, IR, MD2 and HL, and two components of fitness expressed early in life (birth weight and the neonatal mortality of 123 Père David’s deer calves born over six consecutive years). We found that neonatal mortality was 19.1% ± 7.6%, not higher than the 19% or 18% reported in other ungulates. The heterozygosity of calves was not associated with neonatal mortality, nor birth weight. Our study implies that low genetic variability of microsatellite loci has no overt effect on birth weight and neonatal mortality in reintroduced populations of Père David’s deer.

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