Demographic processes underlying subtle patterns of population structure in the scalloped hammerhead shark, Sphyrna lewini

Abstract

Genetic diversity (θ), effective population size (N(e)), and contemporary levels of gene flow are important parameters to estimate for species of conservation concern, such as the globally endangered scalloped hammerhead shark, Sphyrna lewini. Therefore, we have reconstructed the demographic history of S. lewini across its Eastern Pacific (EP) range by applying classical and coalescent population genetic methods to a combination of 15 microsatellite loci and mtDNA control region sequences. In addition to significant population genetic structure and isolation-by-distance among seven coastal sites between central Mexico and Ecuador, the analyses revealed that all populations have experienced a bottleneck and that all current values of θ are at least an order of magnitude smaller than ancestral θ, indicating large decreases in N(e) (θ = 4N(e)μ), where μ is the mutation rate. Application of the isolation-with-migration (IM) model showed modest but significant genetic connectivity between most sampled sites (point estimates of Nm = 0.1-16.7), with divergence times (t) among all populations significantly greater than zero. Using a conservative (i.e., slow) fossil-based taxon-specific phylogenetic calibration for mtDNA mutation rates, posterior probability distributions (PPDs) for the onset of the decline in N(e) predate modern fishing in this region. The cause of decline over the last several thousand years is unknown but is highly atypical as a post-glacial demographic history. Regardless of the cause, our data and analyses suggest that S. lewini was far more abundant throughout the EP in the past than at present.

Figure 1. Map of Eastern Pacific range of Sphyrna lewini and study area.

Sample localities and their associated abbreviations indicated by black dots. The three Panamanian sites are enlarged due to their close proximity to one another.

Figure 2. Haplotype network showing proportion of haplotypes per population.

Haplotypes A and B are common to all populations. Haplotype C is shared by TAR and SCA (hence, the two shades), haplotypes D and E are unique to TAR and CEB, respectively, and haplotypes F and G are unique to SCA. Numbers inside haplotypes C through G indicate the number of haplotypes present in our sampled individuals.

Figure 3. M ratio test results based on microsatellite data for each population.

The population-specific M ratio (open circles), average M from simulations assuming each population is in drift-mutation equilibrium (black circles), and critical M_c based on these simulations (gray circles) are shown. M values below M_c indicate a population has undergone a recent bottleneck. All data shown here were calculated with a proportion of single step mutations (p_s) of 0.90 and an average size of mutations evolving more than one repeat unit (Δ_g) of 3.5. All M values were calculated with θ = 0.01, 0.1, 1.0, and 10.0, corresponding to N_e = 1445, 14,451, 144,509, and 1,445,087, respectively.

Figure 4. Map showing relative migration rates (Nm) between only adjacent pairs of EP populations.

Nm refers to the number of migrants per generation. Red arrows indicate northward gene flow; blue indicate southward flow. Thickness of arrows corresponds to magnitude of flow, or number of migrants per generation. Values in green indicate current N_e, as averaged from estimates of MSVAR and IMa. N_e from IMa was calculated with the equation θ = 4N_eμ.

Figure 5. Posterior probability density of time since divergence for each population pair analyzed in IMa.

The posterior probability density (PPD) of time (t), in years, is based on the fossil-calibrated substitution rate (6.03×10⁻⁹ subs/year).