A novel integrative approach elucidates fine-scale dispersal patchiness in marine populations

Abstract

Dispersal is one of the main determining factors of population structure. In the marine habitat, well-connected populations with large numbers of reproducing individuals are common but even so population structure can exist on a small-scale. Variation in dispersal patterns between populations or over time is often associated to geographic distance or changing oceanographic barriers. Consequently, detecting structure and variation in dispersal on a fine-scale within marine populations still remains a challenge. Here we propose and use a novel approach of combining a clustering model, early-life history trait information from fish otoliths, spatial coordinates and genetic markers to detect very fine-scale dispersal patterns. We collected 1573 individuals (946 adults and 627 juveniles) of the black-faced blenny across a small-scale (2 km) coastline as well as at a larger-scale area (<50 kms). A total of 178 single nucleotide polymorphism markers were used to evaluate relatedness patterns within this well-connected population. In our clustering models we categorized SHORT-range dispersers to be potential local recruits based on their high relatedness within and low relatedness towards other spatial clusters. Local retention and/or dispersal of this potential local recruitment varied across the 2 km coastline with higher frequency of SHORT-range dispersers towards the southwest of the area for adults. An inverse pattern was found for juveniles, showing an increase of SHORT-range dispersers towards the northeast. As we rule out selective movement and mortality from one year to the next, this pattern reveals a complex but not full genetic mixing, and variability in coastal circulation is most likely the main driver of this fine-scale chaotic genetic patchiness within this otherwise homogeneous population. When focusing on the patterns within one recruitment season, we found large differences in temperatures (from approx. 17 °C to 25 °C) as well as pelagic larval duration (PLD) for juveniles from the beginning of the season and the end of the season. We were able to detect fine-scale differences in LONG-range juvenile dispersers, representing distant migrants, depending on whether they were born at the beginning of the season with a longer PLD, or at the end of the reproductive season. The ability to detect such fine-scale dispersal patchiness will aid in our understanding of the underlying mechanisms of population structuring and chaotic patchiness in a wide range of species even with high potential dispersal abilities.

Figure 1

Map of sampling area including the small-scale intensive sampling area (Blanes) and the large-scale collection area. (1) La Pilona, (2) Palomera, (3) Blanes north (4) Clotilde, (5) Lloret de Mar south, (6) Lloret de Mar north, (7) Tossa de Mar. The map was created using ArcGIS 10.5 (www.arcgis.com).

Figure 2

Conceptual Plot showing the four categories of dispersers. Two spatial clusters are represented and the mean relatedness value (r) among the individuals within one cluster (rIN) indicated with a circular arrow and with individuals of other spatial clusters (rOUT) with a straight arrow. The thickness of the lines represents the magnitude: thick = high r, thin = low r.

Figure 3

Spatial clusters within the small-scale area for (a) adults and (b) juveniles. Spatial cluster 6 only exists for the juveniles and few individuals were found. The map was created using ArcGIS 10.5 (www.arcgis.com).

Figure 4

Proportion of adults and juveniles in each spatial cluster (SplClust; Fig. 3) in the SHORT-range disperser category, which are individuals with high mean relatedness with respect to their own spatial cluster (rIN) and low mean relatedness with respect to other spatial clusters (rOUT) as well as LONG-range dispersers, which have low relatedness to all clusters. SplClust6 is not included because it was only found in juveniles and in very low frequency.

Figure 5

Proportion of low dispersers (a) which are individuals with a high relatedness with respect to their own spatial cluster (rIN) and low mean relatedness with respect to other spatial clusters (rOUT) and high dispersers (b) which are individuals with low mean relatedness with respect to all clusters, in early and late juveniles in each spatial cluster (from Fig. 3).

Figure 6

Spatial clusters for juveniles within the whole large-scale area. The map was created using ArcGIS 10.5 (www.arcgis.com).