Against all odds: a tale of marine range expansion with maintenance of extremely high genetic diversity

Abstract

the displacement of species from equatorial latitudes to temperate locations following the increase in sea surface temperatures is among the significant reported consequences of climate change. Shifts in the distributional ranges of species result in fish communities tropicalisation, i.e., high latitude colonisations by typically low latitude distribution species. these movements create new interactions between species and new trophic assemblages. the Senegal seabream, Diplodus bellottii, may be used as a model to understand the population genetics of these invasions. in the last decades, this species has undergone an outstanding range expansion from its African area of origin to the Atlantic coast of the iberian peninsula, where now occurs abundantly. Mitochondrial and nuclear markers revealed a striking high haplotypic nucleotide and genetic diversity values, along with significant population differentiation throughout the present-day geographical range of the Senegal seabream. These results are not consistent with the central-marginal hypothesis, nor with the expectations of a leptokurtic distribution of individuals, as D. bellottii seems to be able to retain exceptional levels of diversity in marginal and recently colonised areas. We discuss possible causes for hyperdiversity and lack of geographical structure and subsequent implications for fisheries. Tropicalisation, the displacement of species from equatorial latitudes to temperate locations, is one of the major reported consequences of climate changes 1-3. The increase of sea surface temperatures (SSTs) in the last decades has promoted shifts in the distributional ranges of species (e.g., 4,5) with individuals moving into areas best corresponding to their physiological optimum. Additionally, the ability of a species to colonise new habitats is influenced by oceanographic currents, the existence of adequate resource availability (i.e., habitat and food) and life-history patterns (e.g., number of eggs produced, age or parental care). These movements lead to the colonization of more poleward habitats by low latitude species, and create new interactions between species and new trophic assemblages. In commercial species, these shifts due to climate change can be magnified by fishing pressures, as reported for the North Sea cod (e.g., 6). Poleward colonization by organisms with a typically equatorial distribution was described almost three decades ago for terrestrial organisms in association with postglacial recolonisation routes (e.g., 7-10). As a general rule, organisms follow a leptokurtic distribution type, in which the majority of individuals stay at or near the original area, and only a fraction disperse to longer distances. This range extension is usually done in a steppingstone manner, implying that each settlement has fewer individuals compared with the previous one. Theoretically, this process corresponds to multiple successive genetic founder events associated with the corresponding genetic implications of the downsize in the effective population num...

Marine Heatwaves Exceed Cardiac Thermal Limits of Adult Sparid Fish (Diplodus capensis, Smith 1884)

“…Range contractions such as this may effectively reduce population sizes and even cause population declines (Neuheimer et al, 2011;Wernberg et al, 2011;Smale and Wernberg, 2013;Deutsch et al, 2015). Poleward expansions of Diplodus populations in response to ocean warming have already been observed for D. bellotti from its endemic origin (Senegal to Cape Blanco in Mauritania) in the West African upwelling region to the Atlantic coast of the Iberian Peninsula (Robalo et al, 2020). A poleward range expansion and an equatorward range contraction was also predicted for D. capensis in the Angola Benguela Frontal Zone (Potts et al, 2014).…”

Genetic hypervariability of a Northeastern Atlantic venomous rockfish

“…Although most locations are represented by numbers of individuals in line with previous phylogeographic studies in marine species, one can a posteriori posit that the high number of singleton haplotypes found is biased by insufficient sampling. In fact, a recent study published by our team recorded even higher genetic diversity in a coastal fish species, revealing that it would be necessary to sample a total of 700 individuals for the sampling to be representative of the population (Robalo et al, 2020). Additionally, we have no samples from intermediate locations between the Atlantic archipelagos and the…”

“…There are two equally possible explanations for this result: (1) if numerous suitable temperature pockets harboured a large enough number of individuals, no demographic bottlenecks would affect the genetic composition and a high genetic variability could be maintained; (2) the species exhibit a patchy distribution near the Macaronesian islands and in scattered locations in the Mediterranean, where self-recruitment may be more dominant than larval drifting to further locations. There are instances where successive self-recruitment generations lead counter-intuitively to the maintenance of high genetic diversity (e.g., Feng, Williams & Place, 2017;Fourdrilis & Backeljau, 2019;Robalo et al, 2020). Furthermore, the CR sequence hypervariability may alternatively or concomitantly be explained by the mutation rate of the fragment, the evolutionary-rates hypothesis, or the metabolic rate theory as discussed in Robalo et al (2020).…”

“…There are instances where successive self-recruitment generations lead counter-intuitively to the maintenance of high genetic diversity (e.g., Feng, Williams & Place, 2017;Fourdrilis & Backeljau, 2019;Robalo et al, 2020). Furthermore, the CR sequence hypervariability may alternatively or concomitantly be explained by the mutation rate of the fragment, the evolutionary-rates hypothesis, or the metabolic rate theory as discussed in Robalo et al (2020).…”

“…One of the evident effects of climate change is the increase in seawater temperature, which translates into a global tropicalization trend (e.g., Bianchi & Morri, 2003;Wernberg et al, 2016) that also affects the Northeastern Atlantic. Along the southern and western coasts of the Iberian Peninsula, several organisms are expanding their poleward distribution, some with great impact in community composition (e.g., Lourenço et al, 2012;Nicastro et al, 2013;Bode et al, 2020;Robalo et al, 2020). One of the fish species recently reported off southwestern continental Portugal is the Madeira rockfish, Scorpaena maderensis Valenciennes 1833 (Encarnação et al, 2019), an estimated moderately vulnerable species (36/100) according to the model by Cheung, Pitcher & Pauly (2005).…”