Genetic relatedness and breeding patterns of a sicklefin lemon shark N. acutidens population in French Polynesia

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In this new paper, we present the result of a 5 year of effort to study the global population structure and behaviour of a small island population of 40 adult sicklefin lemon sharks frequently visiting a provisioning site in Moorea (French Polynesia).

Mourier J, Buray N, Schultz JK, Clua E, Planes S (2013) Genetic Network and Breeding Patterns of a Sicklefin Lemon Shark (Negaprion acutidens) Population in the Society Islands, French Polynesia. PLoS ONE 8(8): e73899. Link

In a first step, we used natural marks on sicklefin lemon shark’s homogeneous body combined with size and sex to identify each individual, describe the population structure and quantify their degree of residency and attachment to the provisioning site by monitoring their occurrence during more than 1000 dives. We then investigated the seasonal individual changes in their visitation patterns as well as the long-term changes in their degree of attachment. We found that the population was composed of different behavioural groups including resident and non-resident sharks. While residents tend to disappear during the mating period, non-residents make some visits during this period. Some residents also appear to increase their degree of attachment to the site along the 5 years of the study.

This increased attachment to the provisioning site led us some interrogation regarding the potential consequences in term of population dynamics and vulnerability for such a small population. As the tourism activity did not appear to modify the “in and out” of males and females from the site for reproduction, and consequently their potential migrations, the next step was to investigate the reproductive biology and population turnover of such poorly known species. We therefore chose to use molecular tools to investigate both the genetic structure of the adult population and its reproduction and recruitment. We therefore started to collect DNA samples from all possible identified sharks. We then explored the island to find potential nursery areas that could offer protection to elusive juvenile sicklefin lemon sharks. We consequently discovered 4 nurseries in Moorea and 3 in the nearby atoll of Tetiaroa. Cohorts of juvenile sharks were therefore caught between 2007 and 2010 in order to get a precious DNA sample.

DNA was sampled on adult lemon sharks using a remote biopsy tip mounted on a speargun as shown in the video below (Note that no sharks were injured during the sampling, they simply came back few minutes after):

We first reconstructed the genetic relationships among adult individuals and created the genetic network which illustrated that all individuals of Moorea and Bora Bora islands, except one, are interconnected at least through one first order genetic relationship. This result highlights that the population is likely relatively small in the region and that sharks migrate across several islands.

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Figure 1: Genetic network of the sicklefin lemon shark population from Moorea and Bora Bora. (A) Map of the study location. (B) The genetic network of adult lemon sharks. Each individual is indicated by a node labelled by shark ID. Circles and squares indicate females and males respectively and symbol size is indicative of the body length of the shark. Node colour corresponds to the three defined residency groups. Dyads sharing a first-order genetic relationship are connected by a line, with line thickness indicating the strength of the genetic relationship (proportional to R values). (C) Genetic degree (number of first-order genetic relationships an individual has) distribution within the population.

We then questioned what the reproductive cycle of this species was. We first monitored the gestation and mating scars of sharks in order to define the mating season as well as the parturition. Male behaviour was also monitored.

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Figure 2. Inference of reproductive cycle from underwater surveys. (A–D) A two-year reproductive cycle as displayed by female F11 which was pregnant in 2007 (A), then entered in a resting period (B) and mated in 2008 as shown by dermal bite wounds on its flanks (C), and was pregnant again in 2009 (D). (E–F) Female F01 is pregnant in 2008 (E) and is followed by males M10 and M31 in a courtship behavior just after parturition in 2008 (F).

Finally, we investigated where the pregnant females we observed gave birth by looking for their progeny in Moorea or Tetiaroa.

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For this, we used parentage analysis by assigning juvenile genotypes back to their parents we sampled in the adult population such as it was also done in its sister species by the Bimini Biological Field Station’s scientists. Except that in our case we mostly assign parentage instead of genetically reconstructing the genotypes of the parents because we have access to the adult stock which is a challenging task as it is necessary to have the DNA of most of juveniles and adults. It resulted in the conclusions that most females showed reproductive philopatry, i.e. they come back to the same nursery for parturition. Females mostly followed a two year reproductive cycle (biennial) as its sister species, although there were some exceptions with females giving birth on two consecutive years (such as F01 in Figure 2). It was also demonstrated multiple paternity in sicklefin lemon sharks as found in most other Carcharhinid species. Finally, while this species developed a clear inbreeding avoidance strategy involving dispersal and migration, we found a low genetic variability and relatively high level of inbreeding compared to other shark studies, which could be due to the low population size and isolation of lemon sharks in islands of French Polynesia.

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