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

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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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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.
... 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. ...
Thesis
Full-text available
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). ...
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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. ...
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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. ...
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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. ...
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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). ...
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• 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. ...
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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. ...
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