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Momigliano, P.

Publications and source records attributed to Momigliano, P..

9 recordsLinked to original sources

Ancient metapopulations and extreme sex-biased demography revealed by ABC inference and X-Chromosome diversity in Indo-Pacific reef sharks

Reconstructing demographic histories in marine species is challenged by extensive geographic distributions, dispersal barriers, high site fidelity, and sex-biased movement. The grey reef shark Carcharhinus amblyrhynchos exemplifies these difficulties: despite limited long-distance dispersal, its Indo-Pacific range spans major oceanographic barriers, leading to competing hypotheses of continuous isolation-by-distance versus hierarchical metapopulation structure. We test these alternatives with a new Approximate Bayesian Computation framework and integrate sex chromosome diversity and differentiation analyses. We find strong support for two ancient, deeply separated Indo-Pacific metapopulations that only recently experienced limited secondary contact. X-chromosome diversity shows extreme reductions relative to autosomes (Q{pi}{approx} 0.18-0.30 in the central/western Indian Ocean and 0.37-0.46 elsewhere), and QFST estimates far below neutral expectations of 0.75. This signature is markedly stronger than in some other carcharhinids and consistent with a reduced effective size of the X chromosome under strong sex-biased dispersal, likely amplified during sequential colonisation events during the last range expansion. Combined evidence of ancient divergence, reduced genetic diversity and extreme depletion of X chromosome diversity supports designating the Western and Central Indian Ocean populations as Evolutionary Significant Units. Our results demonstrate how integrating simulation-based inference with chromosome-specific diversity resolves complex metapopulation histories and reveal how sex-biased dispersal shapes genomic diversity across evolutionary timescales.

evolutionary biology↗

Chromosome-level assembly and annotation of the grey reef shark (Carcharhinus amblyrhynchos) genome

To date only four of nine shark orders have nuclear reference genomes, despite next-generation sequencing advances. Particularly for threatened shark species, there is a lack of reliable genomes which are crucial in facilitating research and conservation applications. We assembled the first nuclear reference genome of the endangered grey reef shark (Carcharhinus amblyrhynchos) using long-read PacBio HiFi and Omni-C sequencing to reach chromosome-level contiguity (36 pseudo chromosomes; 2.9 Gbp) and high completeness (94% complete BUSCOs). BRAKER3 annotated 16,522 protein-coding genes after masking repetitive elements which accounted for 59% of the genome. We identified potential X and Y sex chromosomes on pseudo chromosomes 36 and 57, respectively. The quality and completeness of the draft genome of C. amblyrhynchos suggest that it has the potential to facilitate comprehensive comparative genomics, enabling researchers to investigate genetic variations and adaptations specific to this population and will help advance conservation genetic applications. Significance StatementStemming from an ancient vertebrate lineage, sharks present an interesting evolutionary study system. A third of shark species face extinction, yet critical genomic resources necessary for research and conservation remain scarce. To address this gap, we assembled and annotated the first chromosome-level nuclear reference genome of the threatened grey reef shark (Carcharhinus amblyrhynchos) at high completeness. This genome will help advance studies in evolution, phylogenetics, adaptation, and conservation, offering insights not only for this species but for wider elasmobranch and vertebrate research.

genomics↗

Boundary effects cause false signals of range expansions in population genomic data

Studying range expansions (REs) is central for understanding genetic variation through space and time as well as for identifying refugia and biological invasions. Range expansions are characterized by serial founder events causing clines of decreasing diversity away from the center of origin and asymmetries in the two-dimensional allele frequency spectra. These asymmetries, summarized by the directionality index ({psi}), are sensitive to REs and persist for longer than clines in genetic diversity. In continuous and finite meta-populations, genetic drift tends to be stronger at the edges of the species distribution. Such boundary effects (BEs) are expected to affect geographic patterns in {psi} as well as genetic diversity. With simulations we show that BEs consistently cause high false positive rates in equilibrium meta-populations when testing for REs. In the simulations, the absolute value of {psi} (|{psi}|) in equilibrium data sets was proportional to the fixation index (FST). By fitting signatures of REs as a function of {varepsilon}=|{psi}|/FST and geographic clines in {psi}, strong evidence for REs could be detected in data from a recent rapid invasion of the cane toad, Rhinella marina, in Australia, but not in 28 previously published empirical data sets from Australian scincid lizards or the Indo-Australasian blacktip shark that were significant for the standard RE tests. Thus, while clinal variation in {psi} is still the most sensitive statistic to REs, in order to detect true signatures of REs in natural populations, its magnitude needs to be considered in relation to the overall levels of genetic structuring in the data.

evolutionary biology↗

Determinants of genetic diversity in sticklebacks

Understanding what determines species and population differences in levels of genetic diversity has important implications for our understanding of evolution, as well as for the conservation and management of wild populations. Previous comparative studies have emphasized the roles of linked selection, life-history trait variation and genomic properties, rather than pure demography, as important determinants of genetic diversity. However, these findings are based on coarse estimates across a range of highly diverged taxa, and it is unclear how well they represent the processes within individual species. We assessed genome-wide genetic diversity ({pi}) in 45 nine-spined stickleback (Pungitius pungitius) populations and found that{pi} varied 15-fold among populations ({pi}min{approx}0.00015,{pi} max{approx}0.0023) whereas estimates of recent effective population sizes varied 122-fold. Analysis of inbreeding coefficients (FROH) estimated from runs of homozygosity revealed strong negative association between{pi} and FROH. Genetic diversity was also negatively correlated with mean body size and longevity, but these associations were not statistically significant after controlling for demographic effects (FROH). The results give strong support for the view that populations demographic features, rather than life history differences, are the chief determinants of genetic diversity in the wild.

evolutionary biology↗

Identifying barriers to gene flow and hierarchical conservation units from seascape genomics: a modelling framework applied to a marine predator

The ongoing decline of large marine vertebrates must be urgently mitigated, particularly under increasing levels of climate change and other anthropogenic pressures. However, characterizing the connectivity among populations remains one of the greatest challenges for the effective conservation of an increasing number of endangered species. Achieving conservation targets requires an understanding of which seascape features influence dispersal and subsequent genetic structure. This is particularly challenging for adult-disperser species, and when distribution-wide sampling is difficult. Here, we developed a two-step modelling framework to investigate how seascape features drive the genetic connectivity of marine species without larval dispersal, to better guide the design of marine protected area networks and corridors. We applied this framework to the endangered grey reef shark, Carcharhinus amblyrhynchos, a reef-associated shark distributed across the tropical Indo-Pacific. In the first step, we developed a seascape genomic approach based on isolation-by-resistance models involving circuit theory applied to 515 shark samples, genotyped for 4,491 nuclear single-nucleotide polymorphisms, to explore which parameters drive their population genetic differentiation. We show that deep oceanic areas act as strong barriers to dispersal, while proximity to habitat facilitates dispersal. In the second step, we predicted the resulting genetic differentiation across the entire distribution range of the species, providing both local and global-scale conservation units for future management guidance. We found that grey reef shark populations are more fragmented than expected for such a mobile species, raising concerns about the resilience of isolated populations under high anthropogenic pressures. We recommend the use of this framework to identify barriers to gene flow and to help in the delineation of conservation units at different scales, together with its integration across multiple species when considering marine spatial planning.

ecology↗

Allopatric origin of sympatric whitefish morphs with insights on the genetic basis of their reproductive isolation

The European whitefish (Coregonus lavaretus) species complex is a classic example of recent adaptive radiation. Here we examine a whitefish population introduced to northern Finnish Lake Tsahkal in late 1960s, where three divergent morphs (viz. littoral, pelagic and profundal feeders) were found ten generations after. Using demographic modelling based on genomic data we show that whitefish morphs evolved during a phase of strict isolation, refuting a rapid symmetric speciation scenario. The lake is now an artificial hybrid zone between morphs originated in allopatry. Despite their current syntopy, clear genetic differentiation remains between two of the three morphs. Using admixture mapping three quantitative trait loci associated with gonad weight variation, a proxy for sexual maturity and spawning time, were identified. We suggest that ecological adaptations in spawning time evolved in allopatry are currently maintaining partial reproductive isolation in the absence of other barriers to gene flow.

evolutionary biology↗

Population structure limits parallel evolution

Population genetic theory predicts that small effective population sizes (Ne) and restricted gene flow limit the potential for local adaptation. In particular, the probability of evolving similar phenotypes based on shared genetic mechanisms (i.e. parallel evolution), is expected to be reduced. We tested these predictions in a comparative genomic study of two ecologically similar and geographically co-distributed stickleback species (viz. Gasterosteus aculeatus and Pungitius pungitius). We found that P. pungitius harbours less genetic diversity and exhibits higher levels of genetic differentiation and isolation-by-distance than G. aculeatus. Conversely, G. aculeatus exhibits a stronger degree of genetic parallelism across freshwater populations than P. pungitius: 2996 vs. 379 SNPs located within 26 vs nine genomic regions show evidence of selection in multiple freshwater populations of G. aculeatus and P. pungitius, respectively. Most regions involved in parallel evolution in G. aculeatus showed increased levels of divergence, suggestive of selection on ancient haplotypes. In contrast, regions involved in freshwater adaptation in P. pungitius were younger, and often associated with reduced diversity. In accordance with theory, the results suggest that connectivity and genetic drift play crucial roles in determining the levels and geographic distribution of standing genetic variation, providing evidence that population subdivision limits local adaptation and therefore also the likelihood of parallel evolution.

evolutionary biology↗

Biases in demographic modelling affect our understanding of the process of speciation

Testing among competing demographic models of divergence has become an important component of evolutionary research in model and non-model organisms. However, the effect of unaccounted demographic events on model choice and parameter estimation remains largely unexplored. Using extensive simulations, we demonstrate that under realistic divergence scenarios, failure to account for population size (Ne) changes in daughter and ancestral populations leads to strong biases in divergence time estimates as well as model choice. We illustrate these issues reconstructing the recent demographic history of North Sea and Baltic Sea turbots (Schopthalmus maximus) by testing 16 Isolation with Migration (IM) and 16 Secondary Contact (SC) scenarios, modelling changes in Ne as well as the effects of linked selection and barrier loci. Failure to account for changes in Ne resulted in selecting SC models with long periods of isolation and divergence times preceding the formation of the Baltic Sea. In contrast, models accounting for Ne changes suggest recent (<6 kya) divergence with constant gene flow. We further show how interpreting genomic landscapes of differentiation can help discerning among competing models. For example, in the turbots data islands of differentiation show signatures of recent selective sweeps, rather than old divergence resisting secondary introgression. The results have broad implications for the study of population divergence by high-lighting the potential effects of unmodeleld changes in Ne on demographic inference. Tested models should aim at representing realistic divergence scenarios for the target taxa, and extreme caution should always be exercised when interpreting results of demographic modelling.

evolutionary biology↗

Oceans apart: Heterogeneous patterns of parallel evolution in sticklebacks

An important model system for the study of genomic mechanisms underlying parallel ecological adaptation in the wild is the three-spined stickleback (Gasterosteus aculeatus), which has repeatedly colonized and adapted to freshwater from the sea throughout the northern hemisphere. Previous studies have identified numerous genomic regions showing consistent genetic differentiation between freshwater and marine ecotypes, but these are typically based on limited geographic sampling and are biased towards studies in the Eastern Pacific. We analysed population genomic data from marine and freshwater ecotypes of three-spined sticklebacks with from a comprehensive global collection of marine and freshwater ecotypes to detect loci involved in parallel evolution at different geographic scales. Our findings highlight that most signatures of parallel evolution were unique to the Eastern Pacific. Trans-oceanic marine and freshwater differentiation was only found in a very limited number of genomic regions, including three chromosomal inversions. Using both simulations and empirical data, we demonstrate that this is likely due to both the stochastic loss of freshwater-adapted alleles during founder events during the invasion of the Atlantic basin and selection against freshwater-adapted variants in the sea, both of which have reduced the amount of standing genetic variation available for freshwater adaptation outside the Eastern Pacific region. Moreover, the existence of highly elevated linkage disequilibrium associated with marine-freshwater differentiation in the Eastern Pacific is also consistent with a secondary contact scenario between marine and freshwater populations that have evolved in isolation from each other during past glacial periods. Thus, contrary to what earlier studies focused on Eastern Pacific populations have led us to believe, parallel marine-freshwater differentiation in sticklebacks is far less prevalent and pronounced in all other parts of the species global distribution range.

evolutionary biology↗