Impact of cyclones on hard coral and metapopulation structure, connectivity and genetic diversity of coral reef fish

Cyclones have one of the greatest effects on the biodiversity of coral reefs and the associated species. But it is unknown how stochastic alterations in habitat structure influence metapopulation structure, connectivity and genetic diversity. From 1993 to 2018, the reefs of the Capricorn Bunker Reef group in the southern part of the Great Barrier Reef were impacted by three tropical cyclones including cyclone Hamish (2009, category 5). This resulted in substantial loss of live habitat-forming coral and coral reef fish communities. Within 6–8 years after cyclones had devastated, live hard corals recovered by 50–60%. We show the relationship between hard coral cover and the abundance of the neon damselfish (Pomacentrus coelestis), the first fish colonizing destroyed reefs. We present the first long-term (2008–2015 years corresponding to 16–24 generations of P. coelestis) population genetic study to understand the impact of cyclones on the meta-population structure, connectivity and genetic diversity of the neon damselfish. After the cyclone, we observed the largest change in the genetic structure at reef populations compared to other years. Simultaneously, allelic richness of genetic microsatellite markers dropped indicating a great loss of genetic diversity, which increased again in subsequent years. Over years, metapopulation dynamics were characterized by high connectivity among fish populations associated with the Capricorn Bunker reefs (2200 km2); however, despite high exchange, genetic patchiness was observed with annual strong genetic divergence between populations among reefs. Some broad similarities in the genetic structure in 2015 could be explained by dispersal from a source reef and the related expansion of local populations. This study has shown that alternating cyclone-driven changes and subsequent recovery phases of coral habitat can greatly influence patterns of reef fish connectivity. The frequency of disturbances determines abundance of fish and genetic diversity within species

Living apart together: Long-term coexistence of Baltic cod stocks associated with depth-specific habitat use

Coexistence of fish populations (= stocks) of the same species is a common phenomenon. In the Baltic Sea, two genetically divergent stocks of Atlantic cod (Gadus morhua), Western Baltic cod (WBC) and Eastern Baltic cod (EBC), coexist in the Arkona Sea. Although the relative proportions of WBC and EBC in this area are considered in the current stock assessments, the mixing dynamics and ecological mechanisms underlying coexistence are not well understood. In this study, a genetically validated otolith shape analysis was used to develop the most comprehensive time series of annual stock mixing data (1977–2019) for WBC and EBC. Spatio-temporal mixing analysis confirmed that the two stocks coexist in the Arkona Sea, albeit with fluctuating mixing proportions over the 43-year observation period. Depth-stratified analysis revealed a strong correlation between capture depth and stock mixing patterns, with high proportions of WBC in shallower waters (48–61% in <20m) and increasing proportions of EBC in deeper waters (50–86% in 40-70m). Consistent depth-specific mixing patterns indicate stable differences in depth distribution and habitat use of WBC and EBC that may thus underlie the long-term coexistence of the two stocks in the Arkona Sea. These differences were also reflected in significantly different proportions of WBC and EBC in fisheries applying passive gears in shallower waters (more WBC) and active gears in deeper waters (more EBC). This highlights the potential for fishing gear-specific exploitation of different stocks, and calls for stronger consideration of capture depth and gear type in stock assessments. This novel evidence provides the basis for improved approaches to research, monitoring and management of Baltic cod stocks

Assessing SNP-markers to study population mixing and ecological adaptation in Baltic cod

Atlantic cod (Gadus morhua) is a species of great ecological and economical importance in the Baltic Sea. Here, two genetically differentiated stocks, the western and the eastern Baltic cod, display substantial mechanical mixing, hampering our understanding of cod ecology and impeding stock assessments and management. Based on whole-genome re-sequencing data from reference samples obtained from the study area, we designed two different panels of Single Nucleotide Polymorphisms markers (SNPs), which take into account the exceptional genome architecture of cod. A minimum panel of 20 diagnostic SNPs and an extended panel (20 diagnostic and 18 biologically informative SNPs, 38 in total) were developed and validated to distinguish unambiguously between the western and the eastern Baltic cod stocks and to enable studies of local adaptation to the specific environment in the Baltic Sea, respectively. We tested both panels on cod sampled from the southern Baltic Sea (n = 603) caught in 2015 and 2016. Genotyping results showed that catches from the mixing zone in the Arkona Sea, were composed of similar proportions of individuals of the western and the eastern stock. Catches from adjacent areas to the east, the Bornholm Basin and Gdańsk Deep, were exclusively composed of eastern Baltic cod, whereas catches from adjacent western areas (Belt Sea and Öresund) were composed of western Baltic cod. Interestingly, the two Baltic cod stocks showed strong genetic differences at loci associated with life-history trait candidate genes, highlighting the species’ potential for ecological adaptation even at small geographical scales. The minimum and the extended panel of SNP markers presented in this study provide powerful tools for future applications in research and fisheries management to further illuminate the mixing dynamics of cod in the Baltic Sea and to better understand Baltic cod ecology

<strong>Evidence of hybridization between genetically distinct Baltic cod stocks during peak population abundance(s)</strong>

Range expansions can lead to increased contact of divergent populations, thus increasing the potential of hybridization events. Whether viable hybrids are produced will most likely depend on the level of genomic divergence and associated genomic incompatibilities between the different entities as well as environmental conditions. By taking advantage of historical Baltic cod (Gadus morhua) otolith samples combined with genotyping and whole genome sequencing, we here investigate the genetic impact of the increased spawning stock biomass of the eastern Baltic cod stock in the mid 1980s. The eastern Baltic cod is genetically highly differentiated from the adjacent western Baltic cod, and locally adapted to the brackish environmental conditions in the deeper Eastern basins of the Baltic Sea unsuitable for its marine counterparts. Our genotyping results show an increased proportion of eastern Baltic cod in western Baltic areas (Mecklenburg Bay and Arkona Basin) – indicative of a range expansion westwards – during the peak population abundance in the 1980s. Additionally, we detect high frequencies of potential hybrids (including F1, F2 and backcrosses), verified by whole genome sequencing data for a subset of individuals. Analysis of mitochondrial genomes further indicates directional gene flow from eastern Baltic cod males to western Baltic cod females. Our findings unravel that increased overlap in distribution can promote hybridization between highly divergent populations, and that the hybrids can be viable and survive under specific and favourable environmental conditions. However, the observed hybridization had seemingly no long-lasting impact on the continuous separation and genetic differentiation between the unique Baltic cod stocks.</p

Proportion of WBC in SD 24.

Mixing proportions are based on cod samples from 1st and 4th quarter trawl surveys between 1995 and 2016 (selected years, NOtoliths = 7532). Absolute numbers of otoliths used in the shape analysis are given on the top of each bar. (TIF)</p

Sampling locations of Baltic cod in SD 24.

Cod samples originate from bottom-trawl survey catches (1977 to 2019) and commercial (= com) catches (2010 to 2019) using active (= a) and passive (= p) fishing gears. Inset is a map of the larger Baltic Sea region, indicating ICES subdivisions 22 (Belt Sea), 23 (Øresund), 24 (Arkona Sea) and 25 (Bornholm Basin). Grid within SD 24 represents ICES statistical rectangles. Source of elevation data from [41].</p

Mixing proportions and spawning stock biomass of Baltic cod stocks.

a) Annual mixing proportions of EBC in SD 24 based on cod otoliths (N = 20 302) from trawl surveys between 1977 and 2019 (black bars) and annual proportions of spawning stock biomass (SSB) of EBC on total cod SSB (i.e. SSBEBC+SSBWBC) in the Baltic Sea (red line). b) Correlation analysis of proportion of EBC in SD 24 and proportion of SSB of EBC in the Baltic Sea. WBC = Western Baltic Cod, R = Pearson correlation coefficient. (TIF)</p

Proportion of genetically identified WBC in SD 24.

Mixing proportions are based on genetically validated baseline samples (N = 348) from [29]. Mixing data were grouped by capture depth and used type of fishing gear (active = trawl, passive = mainly gillnet). Absolute numbers of cod samples used for genetic analysis (in bold) and total numbers of fishing hauls used in the stock mixing analysis (in brackets) are given on the top of each bar. Depths without bars = no data available. (TIF)</p

Spatial distribution of stock mixing proportions in SD 24.

Mixing proportions of WBC and EBC are based on cod samples from German commercial catches between 2010 and 2019. Samples from active and passive gear fisheries are marked with black and green outlines, respectively. Only fishing hauls with ≥50 individuals are shown (Ntotal = 10 631 otoliths from 62 sampled hauls).</p

Seasonal proportions of WBC in SD 24.

Mixing proportions are based on cod samples from German commercial catches between 2010 and 2019 (selected years, NOtoliths = 10 924). Active and passive gear samples are pooled. Absolute numbers of otoliths used in the shape analysis are given on the top of each bar. Quarters without bars = no data available. (TIF)</p