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Combining population genomics with demographic analyses highlights habitat patchiness and larval dispersal as determinants of connectivity in coastal fish species.

ABSTRACT: Gene flow shapes spatial genetic structure and the potential for local adaptation. Among marine animals with nonmigratory adults, the presence or absence of a pelagic larval stage is thought to be a key determinant in shaping gene flow and the genetic structure of populations. In addition, the spatial distribution of suitable habitats is expected to influence the distribution of biological populations and their connectivity patterns. We used whole genome sequencing to study demographic history and reduced representation (double-digest restriction associated DNA) sequencing data to analyse spatial genetic structure in broadnosed pipefish (Syngnathus typhle). Its main habitat is eelgrass beds, which are patchily distributed along the study area in southern Norway. Demographic connectivity among populations was inferred from long-term (~30-year) population counts that uncovered a rapid decline in spatial correlations in abundance with distance as short as ~2 km. These findings were contrasted with data for two other fish species that have a pelagic larval stage (corkwing wrasse, Symphodus melops; black goby, Gobius niger). For these latter species, we found wider spatial scales of connectivity and weaker genetic isolation-by-distance patterns, except where both species experienced a strong barrier to gene flow, seemingly due to lack of suitable habitat. Our findings verify expectations that a fragmented habitat and absence of a pelagic larval stage promote genetic structure, while presence of a pelagic larvae stage increases demographic connectivity and gene flow, except perhaps over extensive habitat gaps.

SUBMITTER: Knutsen H

PROVIDER: S-EPMC9311693 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Computing Lagrangian trajectories with ocean circulation models is a powerful way to infer larval dispersal pathways and connectivity. Defining release areas and timing of particles to represent larval habitat realistically is critical to obtaining representative dispersal pathways. However, it is challenging due to spatial and temporal variability in larval density. Forward-tracking particle experiments were conducted to study larval connectivity of four species (neritic or mesopelagic) in the Gulf of Mexico's (GoM) deep-water region. A seasonal climatology coupled with predicted potential larval habitat models based on generalized additive models was used to delimit the particle dispersal origin. Two contrasting mesoscale circulation patterns were examined: (1) high Loop Current (LC) intrusion, absence of recently detached LC anticyclonic eddies (LC-ACE), and no interaction between LC-ACEs and the semi-permanent cyclonic eddy (CE) in the Bay of Campeche (BoC), and (2) limited LC intrusion, a recently detached LC-ACE, and interaction between LC-ACEs and the BoC's CE. To simulate larval transport, virtual larvae were randomly released in the potential habitats and advected for 30 days with the velocity fields of the HYbrid Coordinate Ocean Model with hourly-resolution assimilation. Potential habitat location and size played a major role in dispersal and connectivity. A greater percentage of particles were retained in potential habitats restricted to the southern BoC, suggesting lower connectivity with other GoM regions than those encompassing most of the BoC or the central Gulf. Mesoscale feature interactions in the western GoM and BoC led to greater dispersion along the western basin. By contrast, the absence of ACE-CE interaction in the BoC led to greater retention and less connectivity between the southern and northern GoM. Under high LC intrusion, particles seeded north of the Yucatan Shelf were advected through the Florida Straits and dispersed within the GoM. Coupling potential habitat models with particle experiments can help characterize the dispersal and connectivity of fish larvae in oceanic systems.

Project description: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.

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Combining population genomics with demographic analyses highlights habitat patchiness and larval dispersal as determinants of connectivity in coastal fish species.

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