Kevin A. Feldheim

Larval export from marine reserves and the recruitment benefit for fish and fisheries

Marine reserves, areas closed to all forms of fishing, continue to be advocated and implemented to supplement fisheries and conserve populations. However, although the reproductive potential of important fishery species can dramatically increase inside reserves, the extent to which larval offspring are exported and the relative contribution of reserves to recruitment in fished and protected populations are unknown. Using genetic parentage analyses, we resolve patterns of larval dispersal for two species of exploited coral reef fish within a network of marine reserves on the Great Barrier Reef. In a 1,000 km(2) study area, populations resident in three reserves exported 83% (coral trout, Plectropomus maculatus) and 55% (stripey snapper, Lutjanus carponotatus) of assigned offspring to fished reefs, with the remainder having recruited to natal reserves or other reserves in the region. We estimate that reserves, which account for just 28% of the local reef area, produced approximately half of all juvenile recruitment to both reserve and fished reefs within 30 km. Our results provide compelling evidence that adequately protected reserve networks can make a significant contribution to the replenishment of populations on both reserve and fished reefs at a scale that benefits local stakeholders.

Global phylogeography and seascape genetics of the lemon sharks (genus Negaprion)

Seascapes are complex environments, and populations are often isolated by factors other than distance. Here we investigate the role of coastal habitat preference and philopatry in shaping the distribution and population structure of lemon sharks. The genus Negaprion comprises the amphiatlantic lemon shark (N. brevirostris), with a relict population in the eastern Pacific, and its Indo‐West Pacific sister species, the sicklefin lemon shark (N. acutidens). Analyzing 138 individuals throughout the range of N. brevirostris (N = 80) and N. acutidens (N = 58) at microsatellite loci (nine and six loci, respectively) and the mitochondrial control region, we find evidence of allopatric speciation corresponding to the Tethys Sea closure (10–14 million years ago) and isolation of the eastern Pacific N. brevirostris population via the emergence of the Isthmus of Panama (~3.5 million years ago). There is significant isolation by oceanic distance (R2 = 0.89, P = 0.005), defined as the maximum distance travelled at depths greater than 200 m. We find no evidence for contemporary transatlantic gene flow (m, M = 0.00) across an oceanic distance of ~2400 km. Negaprion acutidens populations in Australia and French Polynesia, separated by oceanic distances of at least 750 km, are moderately differentiated (FST = 0.070–0.087, P≤ 0.001; ΦST = 0.00, P = 0.99), with South Pacific archipelagos probably serving as stepping stones for rare dispersal events. Migration between coastally linked N. brevirostris populations is indicated by nuclear (m = 0.31) but not mitochondrial (m < 0.001) analyses, possibly indicating female natal site fidelity. However, philopatry is equivocal in N. acutidens, which has the lowest control region diversity (h = 0.28) of any shark yet studied. Restricted oceanic dispersal and high coastal connectivity stress the importance of both local and international conservation efforts for these threatened sharks.

RECONSTRUCTION OF PARENTAL MICROSATELLITE GENOTYPES REVEALS FEMALE POLYANDRY AND PHILOPATRY IN THE LEMON SHARK, NEGAPRION BREVIROSTRIS

Abstract Because sharks possess an unusual suite of reproductive characteristics, including internal fertilization, sperm storage, relatively low fecundity, and reproductive modes that range from oviparity to viviparity, they can provide important insight into the evolution of mating systems and sexual selection. Yet, to date, few studies have characterized behavioral and genetic mating systems in natural populations of sharks or other elasmobranchs. In this study, highly polymorphic microsatellite loci were used to examine breeding biology of a large coastal shark, the lemon shark, Negaprion brevirostris, at a tropical lagoon nursery. Over six years, 910 lemon sharks were sampled and genotyped. Young were assigned into sibling groups that were then used to reconstruct genotypes of unsampled adults. We assigned 707 of 735 young sharks to one of 45 female genotypes (96.2%), and 485 (66.0%) were assigned to a male genotype. Adult female sharks consistently returned to Bimini on a biennial cycle to give birth. Over 86% of litters had multiple sires. Such high levels of polyandry raise the possibility that polyandry evolved in viviparous sharks to reduce genetic incompatibilities between mother and embryos. We did not find a relationship between relatedness of mates and the number of offspring produced, indicating that inbreeding avoidance was probably not driving pre‐ or postcopulatory mate choice. Adult male sharks rarely sired more than one litter at Bimini and may mate over a broader geographic area.

When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks

Selection acting on large marine vertebrates may be qualitatively different from that acting on terrestrial or freshwater organisms, but logistical constraints have thus far precluded selection estimates for the former. We overcame these constraints by exhaustively sampling and repeatedly recapturing individuals in six cohorts of juvenile lemon sharks (450 age‐0 and 255 age‐1 fish) at an enclosed nursery site (Bimini, Bahamas). Data on individual size, condition factor, growth rate and inter‐annual survival were used to test the ‘bigger is better’, ‘fatter is better’ and ‘faster is better’ hypotheses of life‐history theory. For age‐0 sharks, selection on all measured traits was weak, and generally acted against large size and high condition. For age‐1 sharks, selection was much stronger, and consistently acted against large size and fast growth. These results suggest that selective pressures at Bimini may be constraining the evolution of large size and fast growth, an observation that fits well with the observed small size and low growth rate of juveniles at this site. Our results support those of some other recent studies in suggesting that bigger/fatter/faster is not always better, and may often be worse.

There and Back Again: A Review of Residency and Return Migrations in Sharks, with Implications for Population Structure and Management

The overexploitation of sharks has become a global environmental issue in need of a comprehensive and multifaceted management response. Tracking studies are beginning to elucidate how shark movements shape the internal dynamics and structure of populations, which determine the most appropriate scale of these management efforts. Tracked sharks frequently either remain in a restricted geographic area for an extended period of time (residency) or return to a previously resided-in area after making long-distance movements (site fidelity). Genetic studies have shown that some individuals of certain species preferentially return to their exact birthplaces (natal philopatry) or birth regions (regional philopatry) for either parturition or mating, even though they make long-distance movements that would allow them to breed elsewhere. More than 80 peer-reviewed articles, constituting the majority of published shark tracking and population genetic studies, provide evidence of at least one of these behaviors in a combined 31 shark species from six of the eight extant orders. Residency, site fidelity, and philopatry can alone or in combination structure many coastal shark populations on finer geographic scales than expected based on their potential for dispersal. This information should therefore be used to scale and inform assessment, management, and conservation activities intended to restore depleted shark populations.

Two decades of genetic profiling yields first evidence of natal philopatry and long‐term fidelity to parturition sites in sharks

Sharks are a globally threatened group of marine fishes that often breed in their natal region of origin. There has even been speculation that female sharks return to their exact birthplace to breed (‘natal philopatry’), which would have important conservation implications. Genetic profiling of lemon sharks (Negaprion brevirostris) from 20 consecutive cohorts (1993–2012) at Bimini, Bahamas, showed that certain females faithfully gave birth at this site for nearly two decades. At least six females born in the 1993–1997 cohorts returned to give birth 14–17 years later, providing the first direct evidence of natal philopatry in the chondrichthyans. Long‐term fidelity to specific nursery sites coupled with natal philopatry highlights the merits of emerging spatial and local conservation efforts for these threatened predators.

Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks

Multiple mating has clear fitness benefits for males, but uncertain benefits and costs for females. We tested for indirect genetic benefits of polyandry in a natural population, by using data from a long‐term genetic and demographic study of lemon sharks (Negaprion brevirostris) at Bimini, Bahamas. To do so, we followed the fates of individuals from six cohorts (450 age‐0 and 254 age‐1 fish) in relation to their individual level of genetic variation, and whether they were from polyandrous or monoandrous litters. We find that offspring from polyandrous litters did not have a greater genetic diversity or greater survival than did the offspring of monoandrous litters. We also find no evidence of positive associations between individual offspring genetic diversity metrics and our surrogate measure of fitness (i.e. survival). In fact, age‐1 individuals with fewer heterozygous microsatellite loci and more genetically similar parents were more likely to survive to age‐2. Thus, polyandry in female lemon sharks does not appear to be adaptive from the perspective of indirect genetic benefits to offspring. It may instead be the result of convenience polyandry, whereby females mate multiply to avoid harassment by males. Our inability to find indirect genetic benefits of polyandry despite detailed pedigree and survival information suggests the need for similar assessments in other natural populations.

Low genetic differentiation across three major ocean populations of the whale shark, Rhincodon typus.

Background Whale sharks are a declining species for which little biological data is available. While these animals are protected in many parts of their range, they are fished legally and illegally in some countries. Baseline biological and ecological data are needed to allow the formulation of an effective conservation plan for whale sharks. It is not known, for example, whether the whale shark is represented by a single worldwide panmictic population or by numerous, reproductively isolated populations. Genetic analysis of population structure is one essential component of the baseline data required for whale shark conservation. Methodology/Principal Findings We have identified 8 polymorphic microsatellites in the whale shark and used these markers to assess genetic variation and population structure in a panel of whale sharks covering a broad geographic region. This is the first record of microsatellite loci in the whale shark, which displayed an average of 9 alleles per locus and mean Ho = 0.66 and He = 0.69. All but one of the eight loci meet the expectations of Hardy-Weinberg equilibrium. Analysis of these loci in whale sharks representing three major portions of their range, the Pacific (P), Caribbean (C), and Indian (I) Oceans, determined that there is little population differentiation between animals sampled in different geographic regions, indicating historical gene flow between populations. FST values for inter-ocean comparisons were low (P×C = 0.0387, C×I = 0.0296 and P×I = −0.0022), and only C×I approached statistical significance (p = 0.0495). Conclusions/Significance We have shown only low levels of genetic differentiation between geographically distinct whale shark populations. Existing satellite tracking data have revealed both regional and long-range migration of whale sharks throughout their range, which supports the finding of gene flow between populations. Whale sharks traverse geographic and political boundaries during their life history and interbreed with animals from distant populations; conservation efforts must therefore target international protection for this species.

A genetic assessment of polyandry and breeding-site fidelity in lemon sharks

We here employ 11 microsatellite markers and recently developed litter reconstruction methods to infer mating system parameters (i.e. polyandry and breeding‐site fidelity) at a lemon shark nursery site in Marquesas Key, Florida. Four hundred and eight juvenile or subadult sharks were genotyped over eight complete breeding seasons. Using this information, we were able to infer family structure, as well as fully or partially reconstruct genotypes of 46 mothers and 163 fathers. Multiple litter reconstruction methods were used, and novel simulations helped define apparent bias and precision of at least some mating system parameters. For Marquesas Key, we find that adult female lemon sharks display high levels of polyandry (81% of all litters sampled) and stronger fidelity to the nursery site than do males. Indeed, few male sharks sired offspring from more than one litter during the course of the study. These findings were quite similar to previous results from another lemon shark nursery site (Bimini, Bahamas), suggesting conserved mating system parameters despite significant variation in early life‐history traits (i.e. body size and growth) among sites. The finding of at least some site fidelity in females also supports the need for careful conservation of each nursery.

Phylogeography of Two Closely Related Indo-Pacific Butterflyfishes Reveals Divergent Evolutionary Histories and Discordant Results from mtDNA and Microsatellites

Marine biogeographic barriers can have unpredictable consequences, even among closely related species. To resolve phylogeographic patterns for Indo-Pacific reef fauna, we conducted range-wide surveys of sister species, the scrawled butterflyfish (Chaetodon meyeri; N = 134) and the ornate butterflyfish (Chaetodon ornatissimus; N = 296), using mitochondrial DNA cytochrome b sequences and 10 microsatellite loci. The former is distributed primarily in the Indian Ocean but also extends to the Line Islands in the Central Pacific, whereas the latter is distributed primarily in the Central-West Pacific (including Hawaii and French Polynesia) but extends to the eastern margin of the Indian Ocean. Analyses of molecular variance and Bayesian STRUCTURE results revealed 1 range-wide group for C. meyeri and 3 groups for C. ornatissimus: 1) eastern Indian Ocean and western Pacific, 2) Central Pacific, and 3) Hawaii. Estimates of the last population expansion were much more recent for C. meyeri (61 500 to 95 000 years) versus C. ornatissimus (184 700 to 286 300 years). Despite similarities in ecology, morphology, life history, and a broadly overlapping distribution, these sister species have divergent patterns of dispersal and corresponding evolutionary history. The mtDNA and microsatellite markers did not provide concordant results within 1 of our study species (C. meyeri), or in 7 out of 12 other cases of marine fishes in the published literature. This discordance renews caution in relying on one or a few markers for reconstructing historical demography.