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Population structure and male-biased dispersal in the short-tail stingray Bathytoshia brevicaudata (Myliobatoidei: Dasyatidae)

DOI:10.1007/s10592-019-01167-3
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Emily Roycroft at Australian National University
Emily Roycroft
Agnes Le Port at James Cook University
Agnes Le Port
Shane D. Lavery
Shane D. Lavery
Shane D. Lavery
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Abstract and Figures

Selective pressures driving dispersal in vagile species often differ between males and females, resulting in sex-biased dispersal. Male-biased dispersal is common in mammals, where there is greater reproductive investment by females, and there is emerging evidence for a similar pattern in elasmobranchs. We examine the population structure of the short-tail stingray (Bathytoshia brevicaudata), a large, viviparous coastal species common in southern hemisphere waters. Using 11 nuclear (nDNA) microsatellite markers from 202 individuals in comparison to mitochondrial (mtDNA) data reported by Le Port and Lavery (J Hered 103:174–185, 2012), we elucidate patterns of dispersal at both southern hemisphere and New Zealand scales. At a global scale, estimates of population differentiation were comparable across marker types (microsatellite FST = 0.148, p < 0.001, mtDNA ϕST = 0.67, p < 0.001). In contrast, New Zealand structure was much weaker for microsatellite markers (FST = 0.0026, p > 0.05) than for mtDNA (ϕST = 0.054, p < 0.05). Female-only data displayed a greater degree of population differentiation from both nDNA and mtDNA compared to male-only data, and population assignment tests indicated that males were significantly more likely to be immigrants to the population from which they were sampled. We estimate that within New Zealand, male-mediated gene flow is at least fivefold greater than female-mediated gene flow. This molecular evidence for sex-biased dispersal in a batoid species adds further support to male-biased dispersal as a recurrent pattern in viviparous elasmobranchs. Many elasmobranch species are vulnerable to extinction, and understanding movement patterns is crucial to management of threatened populations.
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Vol.:(0123456789)
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Conservation Genetics (2019) 20:717–728
https://doi.org/10.1007/s10592-019-01167-3
RESEARCH ARTICLE
Population structure andmale-biased dispersal intheshort-tail
stingray Bathytoshia brevicaudata (Myliobatoidei: Dasyatidae)
EmilyJ.Roycroft1,2,3 · AgnèsLePort4,5 · ShaneD.Lavery1,4
Received: 4 February 2018 / Accepted: 8 March 2019 / Published online: 18 March 2019
© Springer Nature B.V. 2019
Abstract
Selective pressures driving dispersal in vagile species often differ between males and females, resulting in sex-biased dis-
persal. Male-biased dispersal is common in mammals, where there is greater reproductive investment by females, and there
is emerging evidence for a similar pattern in elasmobranchs. We examine the population structure of the short-tail stingray
(Bathytoshia brevicaudata), a large, viviparous coastal species common in southern hemisphere waters. Using 11 nuclear
(nDNA) microsatellite markers from 202 individuals in comparison to mitochondrial (mtDNA) data reported by Le Port and
Lavery (J Hered 103:174–185, 2012), we elucidate patterns of dispersal at both southern hemisphere and New Zealand scales.
At a global scale, estimates of population differentiation were comparable across marker types (microsatellite FST = 0.148,
p < 0.001, mtDNA ϕST = 0.67, p < 0.001). In contrast, New Zealand structure was much weaker for microsatellite markers
(FST = 0.0026, p > 0.05) than for mtDNA (ϕST = 0.054, p < 0.05). Female-only data displayed a greater degree of population
differentiation from both nDNA and mtDNA compared to male-only data, and population assignment tests indicated that
males were significantly more likely to be immigrants to the population from which they were sampled. We estimate that
within New Zealand, male-mediated gene flow is at least fivefold greater than female-mediated gene flow. This molecular
evidence for sex-biased dispersal in a batoid species adds further support to male-biased dispersal as a recurrent pattern in
viviparous elasmobranchs. Many elasmobranch species are vulnerable to extinction, and understanding movement patterns
is crucial to management of threatened populations.
Keywords Dasyatis brevicaudata· Smooth stingray· Coastal stingray· Microsatellite· Population genetics· Sex-biased
dispersal
Introduction
The migration of individuals is the primary mechanism
of gene flow in natural populations, and thus the dispersal
behaviour of species has a direct consequence on their popu-
lation genetic structure (Slatkin 1985). This is highlighted
by the association between the spatial scale of population
genetic structure and dispersal tendencies of taxa, particu-
larly in marine species (Bohonak 1999; Bradbury etal.
2008). Underlying the dispersal behaviour of individuals
is a complex interaction between factors that either pro-
mote dispersal (e.g. kin competition, inbreeding avoidance,
resource availability), or limit dispersal (e.g. mortality costs,
familiarity with natal area, kin cooperation) (reviewed in
Perrin and Mazalov 2000). The balance of selective pres-
sures that underpin dispersal behaviour are variable across
taxa, but can also be variable within species. Sex-biased
dispersal describes a disparity in the tendency or ability of
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s1059 2-019-01167 -3) contains
supplementary material, which is available to authorized users.
* Emily J. Roycroft
emily.roycroft@gmail.com
1 School ofBiological Sciences, University ofAuckland,
Private Bag 92019, Auckland, NewZealand
2 Present Address: Sciences Department, Museums Victoria,
Melbourne, VIC3001, Australia
3 Present Address: School ofBioSciences, University
ofMelbourne, Parkville, VIC3010, Australia
4 Institute ofMarine Science, Leigh Marine Laboratory,
University ofAuckland, PO Box349, Warkworth0941,
NewZealand
5 Centre forSustainable Tropical Fisheries andAquaculture,
James Cook University, Townsville4811, Australia
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Supplementary resources (5)

Roycroft_etal_2019_eSupp_5.pdf
Data
March 2019
Emily Roycroft · Agnes Le Port · Shane D. Lavery
Roycroft_etal_2019_eSupp_4.pdf
Data
March 2019
Emily Roycroft · Agnes Le Port · Shane D. Lavery
Roycroft_etal_2019_eSupp_3.pdf
Data
March 2019
Emily Roycroft · Agnes Le Port · Shane D. Lavery
Roycroft_etal_2019_eSupp_2.pdf
Data
March 2019
Emily Roycroft · Agnes Le Port · Shane D. Lavery
Roycroft_etal_2019_eSupp_1.xlsx
Data
March 2019
Emily Roycroft · Agnes Le Port · Shane D. Lavery
... Genetic investigation has discovered that male-based gene-flow in this species is five-times that of female-based gene flow, and males are more likely to be immigrants into the area where they were sampled (Roycroft et al., 2019). This supports growing evidence that male-biased dispersal is a common strategy in viviparous elasmobranchs (Roycroft et al., 2019). ...
... Genetic investigation has discovered that male-based gene-flow in this species is five-times that of female-based gene flow, and males are more likely to be immigrants into the area where they were sampled (Roycroft et al., 2019). This supports growing evidence that male-biased dispersal is a common strategy in viviparous elasmobranchs (Roycroft et al., 2019). When applying this more recent information to the previous satellite tag based study by Le Port et al. (2008), it might be expected that these sub-adult females did not undergo a long-distance migration. ...
... tenuicaudatus males and females from the offshore samples. This could be attributed to a difference in physiology, with females passing certain metals to their young during gestation (Maternal transfer) (Mathews et al., 2008), or a difference in philopatry and movement habits between sexes as is known for B. brevicaudata (Roycroft et al., 2019). Female teleosts typically have higher levels of Zn and Cu than males due to differences in metabolic demands (Canli & Atli, 2003) and indeed the PCoA analysis in this study found that these metals were driving some of the difference between females and males. ...
The Ecology of Ray Species in an Urbanised Estuary: Seasonality, Habitat use and Pollutant Exposure in Tauranga Harbour
Thesis
Full-text available
  • Feb 2020
Information about the movement, seasonality, and use of habitats by marine animals is vital for the mitigation of potential anthropogenic impacts. Ray species may be particularly at risk as they regularly inhabit coastal and estuarine waters. In New Zealand to-date, there has been scant research on the ecology of native ray species in estuarine habitats. In particular, there is a dearth of knowledge pertaining to the spatio-temporal use of the range of habitats within estuaries. The research detailed in this thesis was aimed at addressing the shortfall of information. First, a review of the methodology utilised in ascertaining movement behaviour in non-shark-like batoid elasmobranch species was carried out, as optimisation of tagging research technique underpins the ability to track behaviour of these organisms for long periods. Most studies reviewed adopted tag anchor techniques used on teleost fishes or sharks. As a consequence, the quality of information pertaining to ray habitat use and movements was, in many circumstances, poor. Synthesis of tag longevity using differing anchor methods and field and aquarium longevity experiments led to a recommendation of nylon umbrella darts for soft-skinned non-shark-like rays such as Bathytoshia brevicaudata. Second, seasonality in habitat use within the Tauranga Harbour system was examined using monthly counts of the feeding excavations of Myliobatis tenuicaudatus. This study expanded previous estimations of seasonality and feeding habitat choice in estuaries. It determined that temperature-mediated sinusoidal seasonal patterns in feeding behaviour over a period of 24 months, differed in magnitude and peak month across a range of spatial scales. This could suggest some form of sequential habitat use. Unlike previous studies, evidence of ray feeding was found year-round. This behavioural pattern has implications for calculations of sediment turnover and transport. Peak turnover estimates of ray origin from this study doubled previous estimated calculations. In addition, infaunal prey density, and locational aspects of estuary ‘sub-habitats’ characterised as various ‘zones’ as compared to ‘harbour basin’ habitats, were all found to be influential in the prediction of M. tenuicaudatus feeding activity. There were inverse seasonal differences in the relationship between densities of large infaunal bivalves (putative prey items) and ray feeding activity, suggesting that during some periods, other prey types (soft bodied organisms) may also be important. Suggestions are made that perceived predator risk and human disturbance may have a role in driving habitat preferences in addition to prey density. This study also found that natural mangrove fringe is preferred by M. tenuicaudatus for feeding habitat over areas of ‘fringe’ that had been trimmed to prevent mangrove spread. The implications of this are significant as there is a reduction in ideal feeding habitat with ongoing mangrove trimming regimes. Finally, quantification of metal body burden of M. tenuicaudatus identified low levels of some heavy metals in rays from Tauranga Harbour when compared to Porirua Harbour, and that metals in rays from the outer coast of the Bay of Plenty region were likely to be of volcanic origin. Significantly different metal assemblages of estuarine and offshore animals combined with feeding evidence found year-round in Tauranga Harbour, suggests a separation in populations between these areas. Overall however, it is clear that metal content in Tauranga Harbour rays lies below FZANZ levels of concern and the harbour may be classified as relatively unpolluted. However, the behavioural patterns of rays clearly lead them away from shallower sub estuary areas, that are known to be more contaminated by anthropogenic activity. In conclusion, this thesis provides previously unknown information about the habits and ecology of the important estuarine mesopredator M. tenuicaudatus in the context of anthropogenic risk associated with an urbanised harbour ecosystem. The information will allow informed management of harbour activities and developmental options with regard to conservation of an ecologically important species.
... The finding of philopatric behaviors in both sexes of elasmobranchs Flowers et al. 2016) is seemingly in contrast to reports of MBD from numerous population structure studies of sharks (e.g. Bernard et al. 2016;Corrigan et al. 2018;Day et al. 2019), and more recently, rays (Phillips et al. 2017;Green et al. 2018;Roycroft et al. 2019), as well as to theory-based predictions. Since the evidence of MBD in elasmobranchs largely comes from studies of population structure and gene flow, a critical review of the methodologies, results, and caveats of the genetic evidence of SBD is needed. ...
... For example, coastal species with large body sizes and vagilities, such as C. plumbeus, Silvertip Shark, Carcharhinus albimarginatus, and G. cuvier show MBD in water depths of \ 500 m (Portnoy et al. 2010;Holmes et al. 2017;Momigliano et al. 2017). The demersal/coastal Short-tail Stingray, Bathytoshia brevicaudata, shows MBD across coastal New Zealand, but both female and male dispersal is restricted between Australia, New Zealand, and eastern Africa, suggesting their dispersal is limited by deepwater habitat (Le Port and Lavery 2012; Roycroft et al. 2019). In contrast, biparental gene flow was found in B. brevicaudata across the south of Australia, although this was based on small sample sizes (Roycroft et al. 2019). ...
... The demersal/coastal Short-tail Stingray, Bathytoshia brevicaudata, shows MBD across coastal New Zealand, but both female and male dispersal is restricted between Australia, New Zealand, and eastern Africa, suggesting their dispersal is limited by deepwater habitat (Le Port and Lavery 2012; Roycroft et al. 2019). In contrast, biparental gene flow was found in B. brevicaudata across the south of Australia, although this was based on small sample sizes (Roycroft et al. 2019). Similarly, MBD was also found in the Leafscale Gulper Shark, Centrophorus squamosus, in New Zealand, but both female and male gene flow was impeded by the Benguela Barrier (Veríssimo et al. 2012); an area of cold-water upwelling near South Africa that limits dispersal between the West Indian and East Atlantic in other warm-water fishes, including R. typus (Castro et al. 2007;Briggs and Bowen 2013). ...
Reviewing the genetic evidence for sex-biased dispersal in elasmobranchs
Article
Full-text available
Dispersal in many organisms is asymmetric by sex, a pattern that is often identified through the use of genetic tools. Sex-biased dispersal (SBD) is thought to derive from the varying fitness needs of females and males, as mediated by local ecology and life history. SBD is frequently reported in elasmobranchs (sharks, rays), long-lived fishes that often give live birth to well-developed young and are capable of dispersing thousands of kilometers. While many studies point to male-biased dispersal (MBD) being common, results are highly variable and no clear trends have yet emerged, even as the number of case studies has grown over the past decade. Here, we evaluated patterns in sampling regime, molecular marker type, and analysis method for every genetic structure study published to date that allowed for an assessment of SBD in elasmobranchs. We find that while some degree of MBD in elasmobranchs is likely, factors such as the pooling of life stages during data analysis and the inherent characteristics of different marker types, may lead to an overemphasis on male dispersal and potentially obscure genetic signals of female and male reproductive philopatry. The role of life history and biogeography in determining patterns of SBD in sharks and rays is also discussed.
... It has only been reported in spotted eagle ray (A. narinari) (Sellas et al. 2015), short-tail stingray (Bathytoshia brevicaudata) (Roycroft et al. 2019), and southern stingray (Hypanus americanus) (Schwanck et al. 2020). The rays generally exhibit K-selected life history characteristics such as longevity, long gestation periods, large ova, and aplacental viviparity (Last et al. 2016a). ...
... Population genetic homogeneity also has been reported from other rays, such as the short-tail stingray (B. abrevicaudata) which is homogeneous along both the coast of Australia and the coast of New Zealand (Roycroft et al. 2019). Whether the larvae and the adults can be carried by the SCC and CCC currents need to be verified with additional ecological investigations. ...
Insights into genetic variation and demographic history of sharpnose rays: Examinations of three species of Telatrygon (Elasmobranchii, Dasyatidae) from the Indo‐West Pacific
Article
Coastal and demersal chondrichthyans (sharks, rays, and skates) are expected to exhibit high levels of genetic differentiation in areas of complex geomorphology. Population genetic studies investigating the extent to which demographic history shapes the genetic structure of these fishes are rare. Here, we combination mitochondrial DNA (Cytb and ND2) and eight nuclear microsatellite loci from 244 individuals to examine the population genetic structure and demographic history of the three Indo-West Pacific species of sharpnose rays (Telatrygon zugei, Telatrygon biasa, and Trygon crozieri). High levels of genetic variation both within and between species was identified. Phylogenetic analysis partitioned haplotypes into two lineages supporting divergence of T. zugei from T. crozieri and T. biasa during the Pleistocene. Furthermore, microsatellite-based clustering analyses identified four genetic groups (i.e., T. zugei from Japan, T. zugei from coastal China, T. biasa from Gulf of Thailand, and T. crozieri from the Andaman Sea. Measurements of genetic differentiation also support these four groups. Additionally, Pleistocene demographic expansions were examined in all genetic groups. The climate oscillations and current hydrologic cycles in the Indo-West Pacific appear to be coincide with the hypothesis regarding speciation and the observed demographic history trends of the sharpnose rays. Considering the species group has, until recently, been thought to be one species, these results are critical for defining management units and guiding conservation efforts to preserve stingray biodiversity. This article is protected by copyright. All rights reserved
... Harbour seals in EI were genetically distinct from harbour seals in NWNI, based on mtDNA (only), and harbour seals in SWI were significantly differentiated from harbour seals in NWNI, based on microsatellite data (only). These inconsistencies between mitochondrial and nuclear markers may be attributed to differing sample sizes (Reiner, Lang & Willems, 2019) or can be indicative of sex-related differences in dispersal and migration (Lyrholm et al., 1999;Escorza-Trevino & Dizon, 2000;Herreman et al., 2009;Sonsthagen et al., 2012;Roycroft, Le Port & Lavery, 2019), considering that mtDNA is inherited maternally and thus reflects gene flow (or lack thereof) in females only. Here, geographic sampling differences between mitochondrial and nuclear data for NWNI exist, with mitochondrial data primarily including samples from NWI, whereas nuclear data include substantially more samples from NI. ...
Population structure and genetic connectivity reveals distinctiveness of Irish harbour seals ( Phoca vitulina ) and implications for conservation management
Article
  • Dec 2022
The identification of discrete intraspecific units, such as genetically informed management units (MUs), is important to effectively develop and implement conservation strategies for protected species. Harbour seals (Phoca vitulina) occurring in Irish waters are currently viewed as a single nationwide panmictic population (and hence MU), although this assumption is not based on any knowledge of population structure because of the lack of available genetic data. Thus, the present study used mitochondrial control region sequences and between nine and 11 microsatellite loci from harbour seals from Ireland and Northern Ireland (up to n = 123) and adjacent UK/European waters (up to n = 289) to provide insights into the genetic population structure and diversity of harbour seals in the areas studied. Within the island of Ireland, genetic analyses revealed the presence of three genetically distinct local populations, characterized by high genetic diversity, hereby defined as: East Ireland (EI), North‐west & Northern Ireland (NWNI), and South‐west Ireland (SWI). Using previously published and newly generated data, a subsequent wider scale analysis revealed that the EI and SWI local populations were genetically distinct from neighbouring UK/European areas, whereas seals from the NWNI area could not be distinguished from a previously identified Northern UK metapopulation. Migration rate estimates showed that NWNI receives migrants from North‐west Scotland, with NWNI acting as a genetic source for both SWI and EI. The present study provides the most comprehensive genetic assessment of harbour seals in European waters to date, with findings indicating that conservation strategies for harbour seals in Irish waters should be amended to accommodate at least three genetically distinct local populations/MUs. The use of approaches considering both ecological and genetic parameters is recommended for future assessments and delineation of units of ecological relevance for conservation management purposes.
... Mito-nuclear discordance has been increasingly found in phylogeographic studies within and among conspecific populations and closely related species (Avise et al. 2016). This intriguing phenomenon may be caused by various biological processes, such as female-linked selection (e.g., Fossøy et al. 2016), sex-biased dispersal (e.g., Roycroft et al. 2019), mitochondrial capture through introgression (e.g., Andersen et al. 2021), and invasions by reproductive parasites (e.g., Wolbachia spp., Arif et al. 2021). In this study, mito-nuclear discordance was mainly observed in the populations located in the hybrid zone, which suggested that the hybrid populations of NMBT and HLQQ incorporating both the western and eastern genetic components detected by the nuclear data were completely grouped into the eastern lineage based on the mitochondrial data. ...
Climate warming since the Holocene accelerates west-east communication for a Eurasian temperate species Aquarius paludum
Article
Full-text available
Holocene climate warming has dramatically altered biological diversity and distributions. Recent human-induced emissions of greenhouse gases will exacerbate global warming and thus induce threats to cold-adapted taxa. However, the impacts of this major climate change on transcontinental temperate species are still poorly understood. Here, we generated extensive genomic datasets for a water strider, Aquarius paludum, which was sampled across its entire distribution in Eurasia and used these datasets in combination with ecological niche modelling (ENM) to elucidate the influence of the Holocene and future climate warming on its population structure and demographic history. We found that A. paludum consisted of two phylogeographic lineages that diverged in the middle Pleistocene, which resulted in a "west-east component" genetic pattern that was probably triggered by Central Asia-Mongoxin aridification and Pleistocene glaciations. The diverged western and eastern lineages had a second contact in the Holocene, which shaped a temporary hybrid zone located at the boundary of the arid-semiarid regions of China. Future predictions detected a potentially novel northern corridor to connect the western and eastern populations, indicating west-east gene flow would possibly continue to intensify under future warming climate conditions. Further integrating phylogeographic and ENM analyses of multiple Eurasian temperate taxa based on published studies reinforced our findings on the "west-east component" genetic pattern and the predicted future northern corridor for A. paludum. Our study provided a detailed paradigm from a phylogeographic perspective of how transcontinental temperate species differ from cold-adapted taxa in their response to climate warming.
... Across the board, detections were lower for males, reflecting a difference between the sexes in terms of the time they spent around receivers and perhaps more widely. In other elasmobranchs, sex-biased dispersal is relatively common and typically involves wider ranging movements in males (Pardini et al., 2001;Daly-Engel et al., 2012;Chin et al., 2013;Portnoy et al., 2015;Roycroft, Le Port & Lavery, 2019). A number of hypotheses might explain this behaviour (Wearmouth & Sims, 2010), such as differing habitat requirements in relation to divergent reproductive strategies (Economakis & Lobel, 1998) and the competitive exclusion of males by larger females (Corcoran et al., 2013). ...
Movement patterns of a Critically Endangered elasmobranch (Dipturus intermedius) in a Marine Protected Area
Article
  • Dec 2021
• Marine Protected Areas (MPAs) are widely used in marine management, but for mobile species understanding the spatio-temporal scale of management measures that is required to deliver conservation benefits depends on a detailed knowledge of species’ movements that is often lacking. This is especially the case for species of skate (Rajidae) for which relatively few movement studies have been conducted. • In Scotland, the Loch Sunart to the Sound of Jura MPA covering 741 km² has been designated for the conservation of the Critically Endangered flapper skate (Dipturus intermedius), but fine-scale movements within this area remain poorly understood. • A passive acoustic telemetry study which coupled acoustic tagging of 42 individuals and a static array of 58 receivers was conducted from March 2016 to June 2017. Using acoustic detection time series, angler capture–recapture data and depth time series from archival tags, fine-scale movements of individuals were investigated. • Overall, 33 of the 42 tagged individuals were detected. Residency, site fidelity and transiency were documented. Residency around receivers, lasting from 3 to more than 12 months, was documented in 16 acoustically detected individuals (48%) and all life-history categories, but was most noticeable among females. Acoustic detections were associated with depth, salinity and season, but there was no evidence that individuals formed close-knit groups in the areas in which they were detected. • Taken together with historical occurrence records of flapper skate, the prevalence and scale of residency documented here suggest that the MPA is sufficiently large to benefit a notable percentage (38 [24–52]%) of skate found in the study area over monthly and seasonal timescales. This result strengthens the case for the use of MPAs to support the conservation of flapper skate and other skate species that display similar movement patterns in areas of high local abundance.
... However, the life cycle and reproductive characteristics of U. cognatus are still poorly known. Although the sex-related dispersal pattern among aquatic organisms has been documented in elasmobranch, horseshoe crab, eels, sea-snake and turtle [67][68][69][70][71] , it has never been reported in stargazer. Thus, more studies on uranoscopids should be conducted to uncover more information on this benthic creature. ...
Genetic diversity, population structure and historical demography of the two-spined yellowtail stargazer (Uranoscopus cognatus)
Article
Full-text available
  • Jun 2021
Benthic species, though ecologically important, are vulnerable to genetic loss and population size reduction due to impacts from fishing trawls. An assessment of genetic diversity and population structure is therefore needed to assist in a resource management program. To address this issue, the two-spined yellowtail stargazer (Uranoscopus cognatus) was collected within selected locations in the Indo-West Pacific (IWP). The partial mitochondrial DNA cytochrome c oxidase subunit 1 and the nuclear DNA recombination activating gene 1 were sequenced. Genetic diversity analyses revealed that the populations were moderately to highly diversified (haplotype diversity, H = 0.490–0.900, nucleotide diversity, π = 0.0010–0.0034) except sampling station (ST) 1 and 14. The low diversity level, however was apparent only in the matrilineal marker (H = 0.118–0.216; π = 0.0004–0.0008), possibly due to stochastic factors or anthropogenic stressors. Population structure analyses revealed a retention of ancestral polymorphism that was likely due to incomplete lineage sorting in U. cognatus, and prolonged vicariance by the Indo-Pacific Barrier has partitioned them into separate stock units. Population segregation was also shown by the phenotypic divergence in allopatric populations, regarding the premaxillary protrusion, which is possibly associated with the mechanism for upper jaw movement in biomechanical feeding approaches. The moderate genetic diversity estimated for each region, in addition to past population expansion events, indicated that U. cognatus within the IWP was still healthy and abundant (except in ST1 and 14), and two stock units were identified to be subjected to a specific resource management program.
... However, there are far fewer studies (e.g. Roycroft et al. 2019) that investigate mating strategies and dispersal behaviors for rays, including natal philopatry (i.e. individuals reproducing in their exact birthplace) and regional philopatry (i.e. ...
Female philopatry in smalltooth sawfish Pristis pectinata: conservation and management implications
Article
Full-text available
  • Jun 2021
Populations are more effectively managed with information on breeding and dispersal behavior, making the evaluation of these characteristics essential for effective conservation of a species. In the USA, 2 critical habitat units were designated in 2009 for the federally endangered smalltooth sawfish Pristis pectinata . Previous research in the Charlotte Harbor Estuary Unit (CHEU) of critical habitat shows that female smalltooth sawfish are polyandrous and highly philopatric to nursery grounds. However, these characteristics have not yet been examined in a larger area of designated critical habitat: the Ten Thousand Islands/Everglades Unit (TTIEU). We used microsatellite genotypes from 214 juvenile smalltooth sawfish to examine mating and dispersal behavior via sibship analyses and reconstruction of parental genotypes with the program COLONY. Parental reconstruction yielded 71 female and 117 male genotypes. Many females returned to the same region within TTIEU for parturition on a biennial cycle; however, at least 1 female switched parturition sites within TTIEU and at least 2 females produced litters in both TTIEU and CHEU over the study period. The maximum number of pups genetically assigned to 1 female was 12, a number that is consistent with that found for CHEU (8 pups), and within the litter size range reported (7 to 14) for the species. Confirmation of these mating behaviors and reproductive characteristics is important for understanding how the present population uses these protected habitats at different life stages, and for determining future habitat protection and population expansion strategies to restore smalltooth sawfish to previously occupied areas of their range.
From rivers to ocean basins -Quantifying sex-specific connectivity in sharks
Thesis
Full-text available
  • May 2021
Globally, elasmobranch populations (sharks and rays) are declining due to increasing anthropogenic and climate pressures. Genetic connectivity between elasmobranch populations is crucial to ensure their persistence and sustain the ecological integrity of ecosystems. Genetic connectivity implies gene flow among discrete populations occurring via the dispersal of individuals outside their population of origin, followed by reproduction — a process that can be biased between sexes (i.e. sex-biased dispersal or SBD). In this thesis, I first examine the current knowledge of population structure and SBD in elasmobranchs, and the tools that are commonly used. Next, this thesis uses novel genomic approaches (kinship, nuclear single nucleotide polymorphisms, and mitochondrial genomes) to provide insights into the patterns of (i) population structure, (ii) sex-chromosome systems, and (iii) SBD in elasmobranchs. My thesis focuses on three shark species that allow the study of dispersal patterns based on life history, local ecology, population size and different seascape features: Northern River Shark, Glyphis garricki; School Shark, Galeorhinus galeus; and Bull Shark, Carcharhinus leucas. Overall, male-biased dispersal (MBD) was observed in 25 of the 50 studied species. Population structure was found at both broad (Bull Shark) and fine (Northern River Shark) spatial scales. I demonstrated that 19 out of the 21 studied elasmobranch species contain X and Y chromosomes using the R function I developed. Combined, the sex-linked markers and kinship data supported the evidence of MBD in the Northern River Shark and the Bull Shark. My final discussion synthesised the observed dispersal patterns and examines the potential ecological and evolutionary drivers for these patterns. I critically compared the genetic and analytical approaches for the detection of population structure and SBD. Finally, potential implications of these quantitative findings for management were highlighted.
Rangewide Population Structure of the Clearnose Skate
Article
  • Mar 2022
Skates (family Rajidae) are benthic elasmobranchs that are highly vulnerable to incidental fishery bycatch, are discarded at sea, and are poorly accounted for in catch records. Many aspects of skate life history, such as population structure, are not well understood. Without this knowledge, indiscriminate removal may have deleterious effects on scientific, conservation, and management efforts. The Clearnose Skate Rostroraja eglanteria is seasonally migratory and widely distributed in the coastal waters of the eastern United States and in the northeastern Gulf of Mexico. This study used molecular techniques to assess the population structure of Clearnose Skate for use as a biological reference point for further research and management. Specimens were collected from 2014 to 2019 by fisheries‐independent surveys. High‐throughput genotyping‐by‐sequencing was used to identify single nucleotide polymorphisms, resulting in two data sets: one consisting of 8,914 loci (outlier and neutral) and the other comprised of 30 outlier loci. Results from all analyses and using both data sets indicated a high level of genetic differentiation between specimens from the Gulf of Mexico and specimens from the U.S East Coast. Using the outlier data set, a low but significant level of genetic differentiation was also found among specimens from the U.S. East Coast, with a subtle break near the North Carolina and South Carolina border. Genetic differences along the U.S. East Coast were spatially autocorrelated, indicating a latitudinal genetic gradient. The level of observed genetic differentiation between the Gulf of Mexico and the U.S. East Coast is likely due to physical barriers such as Florida and the Gulf Stream current, while the subtle structure along the U.S. East Coast is likely attributable to isolation caused by dispersal limitations and local temperature preferences. The results from this investigation of Clearnose Skate population structure can be used to better monitor and manage this vulnerable elasmobranch.
Extinction risk and conservation of the world's sharks and rays
Article
Full-text available
The rapid expansion of human activities threatens ocean-wide biodiversity. Numerous marine animal populations have declined, yet it remains unclear whether these trends are symptomatic of a chronic accumulation of global marine extinction risk. We present the first systematic analysis of threat for a globally distributed lineage of 1,041 chondrichthyan fishes-sharks, rays, and chimaeras. We estimate that one-quarter are threatened according to IUCN Red List criteria due to overfishing (targeted and incidental). Large-bodied, shallow-water species are at greatest risk and five out of the seven most threatened families are rays. Overall chondrichthyan extinction risk is substantially higher than for most other vertebrates, and only one-third of species are considered safe. Population depletion has occurred throughout the world's ice-free waters, but is particularly prevalent in the Indo-Pacific Biodiversity Triangle and Mediterranean Sea. Improved management of fisheries and trade is urgently needed to avoid extinctions and promote population recovery.
Mixed-marker approach suggests maternal philopatry and sex-biased behaviours of narrow sawfish Anoxypristis cuspidata
Article
Full-text available
  • Sep 2018
The narrow sawfish Anoxypristis cuspidata belongs to the most endangered family of chondrichthyan fishes, the sawfishes (Pristidae). This species has undergone significant de - clines in geographic range and abundance due to anthropogenic activities including fishing and habitat destruction. Very little is known of adult movements within its distribution. In order to better manage and protect this endangered species, understanding patterns of habitat use, connectivity and behaviour is important. Using a combination of partial mitochondrial sequences (control region [CR] and NADH dehydrogenase 4 [ND4]) and nuclear markers (microsatellites), this study assessed the genetic population structure of A. cuspidata in Australia and Papua New Guinea. Significant population structuring using mitochondrial DNA was found between the east Australian coast, Gulf of Papua and Gulf of Carpentaria (using concatenated CR and ND4 markers) (analysis of molecular variance [AMOVA], ΦST = 0.082, p = < 0.001). In contrast, no population structure was evident across northern Australia using nuclear microsatellite loci (FST = 0.012, p = 1.000). Our results suggest that a combination of historic genetic drift, maternal natal philopatry and possible male-biased dispersal likely drive the genetic patterns observed. Given the endangered status and lack of knowledge for A. cuspidata, this study presents important insights that may be used to inform management efforts.
Population genetics of Southern Hemisphere tope shark (Galeorhinus galeus): Intercontinental divergence and constrained gene flow at different geographical scales
Article
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The tope shark (Galeorhinus galeus Linnaeus, 1758) is a temperate, coastal hound shark found in the Atlantic and Indo-Pacific oceans. In this study, the population structure of Galeorhinus galeus was determined across the entire Southern Hemisphere, where the species is heavily targeted by commercial fisheries, as well as locally, along the South African coastline. Analysis was conducted on a total of 185 samples using 19 microsatellite markers and a 671 bp fragment of the NADH dehydrogenase subunit 2 (ND2) gene. Across the Southern Hemisphere, three geographically distinct clades were recovered, including one from South America (Argentina, Chile), one from Africa (all the South African collections) and an Australia-New Zealand clade. Nuclear data revealed significant population subdivisions (FST = 0.192 to 0.376, p
Mechanisms of peripheral phylogeographic divergence in the indo-Pacific: Lessons from the spiny lobster Panulirus homarus
Article
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Background: There is increasing recognition of the concordance between marine biogeographic and phylogeographic boundaries. However, it is still unclear how population-level divergence translates into species-level divergence, and what are the principal factors that first initiate that divergence, and then maintain reproductive isolation. This study examines the likely forces driving population and lineage divergences in the broadly-distributed Indo-Pacific spiny lobster Panulirus homarus, which has peripheral divergent lineages in the west and east. The study focuses particularly on the West Indian Ocean, which is emerging as a region of unexpected diversity. Mitochondrial control region (mtCR) and COI sequences as well as genotypes of 9 microsatellite loci were examined in 410 individuals from 17 locations grouped into 7 regions from South Africa in the west, and eastward across to Taiwan and the Marquesas Islands. Phylogenetic and population-level analyses were used to test the significance and timing of divergences and describe the genetic relationships among populations. Results: Analyses of the mtCR revealed high levels of divergence among the seven regions (ФST = 0.594, P < 0.001). Microsatellite analyses also revealed significant divergence among regions, but at a much lower level (FST = 0.066, P < 0.001). The results reveal different patterns of mtCR v. nDNA divergence between the two distinct peripheral lineages: a subspecies in South Africa and Madagascar, and a phylogeographically diverged population in the Marquesas. The results also expose a number of other more fine-scale population divergences, particularly in the Indian Ocean. Conclusions: The divergence of peripheral lineages in the west and east of the species' range appear to have been initiated and maintained by very different processes. The pattern of mitochondrial and nuclear divergence of the western lineage, implicates processes of parapatric isolation, secondary contact and introgression, and suggests possible maintenance through adaptation and behavioural reproductive isolation. In contrast, the eastern lineage appears to have diverged through a rare colonisation event, maintained through long-term isolation, and matches expectations of the core-periphery hypothesis. The process of active peripheral speciation may be a common force in the Indo-Pacific that helps drive some of the regions' recognized biogeographic boundaries.
Siting marine protected areas based on habitat quality and extent provides the greatest benefit to spatially structured metapopulations
Article
Full-text available
  • Nov 2016
Siting marine protected areas based on habitat quality and extent provides the greatest benefit to spatially structured metapopulations. Ecosphere 7(11): Abstract. Connectivity and its role in the persistence and sustainability of marine metapopulations are attracting increased attention from the scientific community and coastal resource managers. Whether protection should prioritize the connectivity structure or demographic characteristics of a given patch is still unclear. We design a three-stage population model to analyze the relative importance of sources, sinks, quality and extent of juvenile and adult habitat, and node centralities (eigenvector, degree, closeness, and betweenness) as a basis for prioritizing sites. We use a logistic-type stage-structured model to describe the local dynamics of a population with a sessile adult stage and network models to elucidate propagule-exchange dynamics. Our results show that the coupled states of habitat extent and quality, which determine population carrying capacity, are good criteria for protection strategy. Protecting sites on the basis of sources, sinks, or other centrality measures of connectivity becomes optimal only in limited situations, that is, when larval production is not dependent on the adult population. Our findings are robust to a diverse set of larval pathway structures and levels of larval retention, which indicates that the network topology may not be as important as carrying capacity in determining the fate of the metapopulation. Protecting extensive, good quality habitat can help achieve both conservation and fisheries objectives.
A review of batoid philopatry, with implications for future research and population management
Article
Full-text available
  • Dec 2016
Animal movements, in particular residency or return migrations (collectively defined as ‘philopatry’), can shape population structure and have implications for management. This review examines the evidence for philopatry in batoids, which are some of the least understood and most threatened vertebrates, and updates a prior review of the same in sharks. Evidence for philopatry in batoids was found in 46 studies, including 31 species that involve 11 species complexes. Batoid philopatry research has lagged behind shark philopatry research, with the annual publication rate of shark philopatry studies in the last 5 yr (17 yr-1) being more than twice that of batoids (7 yr-1). Philopatry research on both sharks and rays is taxonomically skewed: <50% of elasmobranch families are represented. Research is also skewed towards charismatic megafauna (white sharks, whale sharks, and manta rays), while the batoid philopatry literature is biased towards ‘Near Threatened’ species, even though approx. 47.5% of batoids are considered to be ‘Data Deficient’ by the IUCN. Limited evidence was found for residency in batoids, contrary to popular assumptions that they are sedentary, and there was limited evidence for sex-differentiated movements. Hypothesis-driven research, longer study durations, more taxon and life stage diverse studies, and consistent use of philopatry terminology are needed to advance the fields of batoid philopatry and conservation. Given strong evidence of philopatry in some species of batoids, management should proceed at the local scale until more studies are conducted.
Challenges and Priorities in Shark and Ray Conservation
Article
Sharks, rays, and chimaeras (Class Chondrichthyes; herein ‘sharks’) are the earliest extant jawed vertebrates and exhibit some of the greatest functional diversity of all vertebrates. Ecologically, they influence energy transfer vertically through trophic levels and sometimes trophic cascades via direct consumption and predation risk. Through movements and migrations, they connect horizontally and temporally across habitats and ecosystems, integrating energy flows at large spatial scales and across time. This connectivity flows from ontogenetic growth in size and spatial movements, which in turn underpins their relatively low reproductive rates compared with other exploited ocean fishes. Sharks are also ecologically and demographically diverse and are taken in a wide variety of fisheries for multiple products (e.g. meat, fins, teeth, and gills). Consequently, a range of fisheries management measures are generally preferable to ‘silver bullet’ and ‘one size fits all’ conservation actions. Some species with extremely low annual reproductive output can easily become endangered and hence require strict protections to minimize mortality. Other, more prolific species can withstand fishing over the long term if catches are subject to effective catch limits throughout the species’ range. We identify, based on the IUCN Red List status, 64 endangered species in particular need of new or stricter protections and 514 species in need of improvements to fisheries management. We designate priority countries for such actions, recognizing the widely differing fishing pressures and conservation capacity. We hope that this analysis assists efforts to ensure this group of ecologically important and evolutionarily distinct animals can support both ocean ecosystems and human activities in the future.
Sex-Biased Survival and Philopatry in Birds: Do they interact?
Article
  • Dec 2016
A review of studies of sex-biased dispersal and philopatry and sex-biased survival in birds is presented. The comparison between sex-related mortality and natal and breeding dispersal at the species-level shows that dispersing birds (mainly females) suffer higher mortality, while philopatric birds (mainly males) have higher survival. The interaction between sex-biased survival and spatial behavior is a crucial component of avian vital strategy, which determine population dynamics and genetic structure.
Inference of Population Structure Using Multilocus Genotype Data
Article
We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.