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- Linking ecology to genetics to better understand adaptation and evolution: a review in marine macrophytesPublication . Hu, Zi-Min; Zhong, Kai-Le; Weinberger, Florian; Duan, De-Lin; Draisma, Stefano G. A.; Serrao, EsterEcological processes and intra-specific genetic diversity reciprocally affect each other. While the importance of uniting ecological variables and genetic variation to understand species’ plasticity, adaptation, and evolution is increasingly recognized, only few studies have attempted to address the intersection of population ecology and genetics using marine macrophyte as models. Representative empirical case studies on genetic diversity are reviewed that explore ecological and evolutionary processes in marine macrophytes. These include studies on environment-induced phenotypic plasticity and associated ecological adaptation; population genetic variation and structuring driven by ecological variation; and ecological consequences mediated by intraspecific and interspecific diversity. Knowledge gaps are also discussed that impede the connection of ecology and genetics in macrophytes and possible approaches to address these issues. Finally, an eco-evolutionary perspective is advocated, by incorporating structural-tofunctional genomics and life cycle complexity, to increase the understanding of the adaptation and evolution of macrophytes in response to environmental heterogeneity.
- Habitat continuity and stepping-stone oceanographic distances explain population genetic connectivity of the brown alga Cystoseira amentaceaPublication . Buonomo, Roberto; Assis, J.; Fernandes, Francisco; Engelen, Aschwin H.; Airoldi, Laura; Serrao, Ester A.Effective predictive and management approaches for species occurring in a metapopulation structure require good understanding of interpopulation connectivity. In this study, we ask whether population genetic structure of marine species with fragmented distributions can be predicted by stepping-stone oceanographic transport and habitat continuity, using as model an ecosystem-structuring brown alga, Cystoseira amentacea var. stricta. To answer this question, we analysed the genetic structure and estimated the connectivity of populations along discontinuous rocky habitat patches in southern Italy, using microsatellite markers at multiple scales. In addition, we modelled the effect of rocky habitat continuity and ocean circulation on gene flow by simulating Lagrangian particle dispersal based on ocean surface currents allowing multigenerational stepping-stone dynamics. Populations were highly differentiated, at scales from few metres up to thousands of kilometres. The best possible model fit to explain the genetic results combined current direction, rocky habitat extension and distance along the coast among rocky sites. We conclude that a combination of variable suitable habitat and oceanographic transport is a useful predictor of genetic structure. This relationship provides insight into the mechanisms of dispersal and the role of life-history traits. Our results highlight the importance of spatially explicit modelling of stepping-stone dynamics and oceanographic directional transport coupled with habitat suitability, to better describe and predict marine population structure and differentiation. This study also suggests the appropriate spatial scales for the conservation, restoration and management of species that are increasingly affected by habitat modifications.
- High and distinct range-edge genetic diversity despite local bottlenecksPublication . Assis, J.; Castilho Coelho, N.; Alberto, F.; Valero, Myriam; Raimondi, P. T.; Reed, D. C.; Serrão, EsterThe genetic consequences of living on the edge of distributional ranges have been the subject of a largely unresolved debate. Populations occurring along persistent low latitude ranges (rear-edge) are expected to retain high and unique genetic diversity. In contrast, currently less favourable environmental conditions limiting population size at such range-edges may have caused genetic erosion that prevails over past historical effects, with potential consequences on reducing future adaptive capacity. The present study provides an empirical test of whether population declines towards a peripheral range might be reflected on decreasing diversity and increasing population isolation and differentiation. We compare population genetic differentiation and diversity with trends in abundance along a latitudinal gradient towards the peripheral distribution range of Saccorhiza polyschides, a large brown seaweed that is the main structural species of kelp forests in SW Europe. Signatures of recent bottleneck events were also evaluated to determine whether the recently recorded distributional shifts had a negative influence on effective population size. Our findings show decreasing population density and increasing spatial fragmentation and local extinctions towards the southern edge. Genetic data revealed two well supported groups with a central contact zone. As predicted, higher differentiation and signs of bottlenecks were found at the southern edge region. However, a decrease in genetic diversity associated with this pattern was not verified. Surprisingly, genetic diversity increased towards the edge despite bottlenecks and much lower densities, suggesting that extinctions and recolonizations have not strongly reduced diversity or that diversity might have been even higher there in the past, a process of shifting genetic baselines.
- Population genetics of Zostera noltii along the west Iberian coast: Consequences of small population size, habitat discontinuity and near-shore currentsPublication . Diekmann, O. E.; Coyer, J. A.; Ferreira, J.; Olsen, J. L.; Stam, W. T.; Pearson, G. A.; Serrão, EsterThe effects of oceanographic patterns on marine genetic biodiversity along the SW Iberian Peninsula are poorly understood. We addressed the question of whether gene flow in this region depends solely on geographic distance between isolated patches of suitable habitat or if there are superimposed effects correlated with other factors such as current patterns. Zostera noltii, the dwarf eelgrass, is the keystone habitat-structuring seagrass species on intertidal mudflats along the Iberian west coast. We used 9 microsatellite loci to analyze population genetic diversity and differentiation for all existing 8 populations from NW Spain (Ria de Vigo) to SW Spain (Puerto Real, Cadiz). Populations are highly genetically differentiated as shown by high significant FST,Wright’s fixation index, (0.08 to 0.26) values. A neighbor-joining tree based on Reynold’s distances computed from allele frequencies revealed a split between northern and southern populations (bootstrap support of 84%). This pattern of differentiation can be explained by (1) ocean surface current patterns present during Z. noltii’s reproductive season which cause a dispersal barrier between the northern and southern populations of this region, (2) habitat isolation, due to large geographic distances between suitable habitats, preventing frequent gene flow, and (3) small effective population sizes, causing high drift and thus faster differentiation rates.
- Oceanographic conditions limit the spread of a marine invader along Southern African shoresPublication . Assis, J.; Zupan, Mirta; Nicastro, Katy; Zardi, Gerardo I.; McQuaid, Christopher D.; Serrao, Ester A.Invasive species can affect the function and structure of natural ecological communities, hence understanding and predicting their potential for spreading is a major ecological challenge. Once established in a new region, the spread of invasive species is largely controlled by their dispersal capacity, local environmental conditions and species interactions. The mussel Mytilus galloprovincialis is native to the Mediterranean and is the most successful marine invader in southern Africa. Its distribution there has expanded rapidly and extensively since the 1970s, however, over the last decade its spread has ceased. In this study, we coupled broad scale field surveys, Ecological Niche Modelling (ENM) and Lagrangian Particle Simulations (LPS) to assess the current invaded distribution of M. galloprovincialis in southern Africa and to evaluate what prevents further spread of this species. Results showed that all environmentally suitable habitats in southern Africa have been occupied by the species. This includes rocky shores between Rocky Point in Namibia and East London in South Africa (approx. 2800 km) and these limits coincide with the steep transitions between cool-temperate and subtropical-warmer climates, on both west and southeast African coasts. On the west coast, simulations of drifting larvae almost entirely followed the northward and offshore direction of the Benguela current, creating a clear dispersal barrier by advecting larvae away from the coast. On the southeast coast, nearshore currents give larvae the potential to move eastwards, against the prevalent Agulhas current and beyond the present distributional limit, however environmental conditions prevent the establishment of the species. The transition between the cooler and warmer water regimes is therefore the main factor limiting the northern spread on the southeast coast; however, biotic interactions with native fauna may also play an important role.
- Population level variation in reproductive development and output in the golden kelp Laminaria ochroleuca under marine heat wave scenariosPublication . Strasser, Fiona-Elaine; Barreto, Luis M.; Kaidi, Soukaina; Sabour, Brahim; A, Serrão; Pearson, Gareth; Martins, NeusaThermal tolerance is often interpreted as a species-wide thermal niche in the absence of studies focusing on the adaptive potential of populations to exhibit differential thermal tolerance. Thus, considering intraspecific thermal plasticity, local adaptation or both between populations along distributional gradients when interpreting and predicting species responses to warming is imperative. Removing the effect of environmental histories by raising kelp gametophyte generations in vitro under common garden conditions allows unbiased comparison between population-specific adaptive variation under different environmental conditions. Following this approach, this study aims to detect (potentially) adaptive differentiation in microscopic life-stages (gametophytes) between populations of a temperate forest forming kelp, Laminaria ochroleuca from locations with distinct thermal conditions. Gametophytes from four geographically distinct populations were subjected to different temperature treatments (17, marine heat waves of 23, 25 and 27 degrees C) and gametophyte survival during thermal stress as well as reproductive success and photosynthetic responses during recovery were investigated. Intraspecific variation in resilience and reproductive output to thermal stress was found in L. ochroleuca; gametophytes from the most northern population (Brittany, France) were the most thermally sensitive, with mortality onset at 23 degrees C, whereas mortality in the remaining populations was only apparent at 27 degrees C. Gametophytes from northern Spain and Morocco exhibited very low reproductive success during recovery from 23 and 25 degrees C. However, when recovering from the highest thermal treatment (27 degrees C) the reproductive development and sporophyte output was higher than in the gametophytes from France and Italy (Mediterranean). The population-specific responses of gametophyte resilience and reproductive success to temperature stress suggest genetic differentiation in response to variation in local thermal regimes.
- Fast sporophyte replacement after removal suggests banks of latent microscopic stages of Laminaria Ochroleuca (phaeophyceae) in tide pools in northern PortugalPublication . Barradas, Ana; Alberto, F.; Engelen, Aschwin; Serrão, EsterThis study investigated the effects of a physical disturbance consisting of the removal of adult kelps (Laminaria ochroleuca Bachelot de la Pylaie)and their corresponding understorey turf assemblage in tide pools in northern Portugal.
- Setting preliminary biometric baselines for new target sea cucumbers species of the NE Atlantic and Mediterranean fisheriesPublication . González-Wangüemert, Mercedes; Valente, Sara; Henriques, Filipe; Domínguez-Godino, Jorge A.; Serrao, EsterCommercial interest on sea cucumber species from the NE Atlantic and the Mediterranean is increasing.Holothuria polii, Holothuria tubulosa, Holothuria mammata and Holothuria arguinensis are the new targetspecies. The scarce biological and ecological knowledge on these species along their geographical distri-bution, is a major problem for their fisheries management. To address it, we carried out a morphometricstudy to describe the baseline population size structure, focused on the length–weight relationship andsize–weight distribution.In the NE Atlantic, the largest mean size and heaviest mean weight of H. mammata and H. arguinensiswere found in localities with upwelling, but another factors could be influencing on these results. In theMediterranean, Girona and Mallorca showed the heaviest specimens of H. polii, H. tubulosa and H. mam-mata, and the smallest were registered in Crete and Kusadasi. Significant differences in length and weightbetween populations were found for each species. These results could be linked with local environmentalconditions. Size frequency distribution was multimodal for all species except for H. mammata; the weightfrequency distribution was only unimodal for H. polii and H. mammata.This study provides novel data, helpful for stock and population assessment which could support theimplementation of effective management for the European sea cucumber target species.
- Fine‐scale genetic structure and flowering output of the seagrass Enhalus acoroides undergoing disturbancePublication . Yu, Shuo; Wu, Yunchao; Serrao, Ester A.; Zhang, Jingping; Jiang, Zhijian; Huang, Chi; Cui, Lijun; Thorhaug, Anitra; Huang, XiaopingSeagrass are under great stress in the tropical coast of Asia, where Enhalus acoroides is frequently the dominant species with a large food web. Here, we investigate the question of the fine-scale genetic structure of this ecologically important foundation species, subject to severe anthropogenic disturbance in China. The genetic structure will illuminate potential mechanisms for population dynamics and sustainability, which are critical for preservation of biodiversity and for decision-making in management and restoration. We evaluated the fine-scale spatial genetic structure (SGS) and flowering output of E. acoroides, and indirectly estimated the relative importance of sexual versus asexual reproduction for population persistence using spatial autocorrelation analysis. Results reveal high clonal diversity for this species, as predicted from its high sexual reproduction output. The stronger Sp statistic at the ramet-level compared with genet-level indicates that clonality increases the SGS pattern for E. acoroides. Significant SGS at the genet-level may be explained by the aggregated dispersal of seed/pollen cohorts. The estimated gene dispersal variance suggests that dispersal mediated by sexual reproduction is more important than clonal growth in this study area. The ongoing anthropogenic disturbance will negatively affect the mating pattern and the SGS patterns in the future due to massive death of shoots, and less frequency of sexual reproduction.
- Mates matter: gametophyte kinship recognition and inbreeding in the giant kelp, Macrocystis pyrifera (Laminariales, Phaeophyceae)Publication . Camus, Carolina; Solas, Maribel; Martinez, Camila; Vargas, Jaime; Garces, Cristobal; Gil-Kodaka, Patricia; Ladah, Lydia B.; Serrao, Ester A.; Faugeron, SylvainInbreeding, the mating between genetically related individuals, often results in reduced survival and fecundity of offspring, relative to outcrossing. Yet, high inbreeding rates are commonly observed in seaweeds, suggesting compensatory reproductive traits may affect the costs and benefits of the mating system. We experimentally manipulated inbreeding levels in controlled crossing experiments, using gametophytes from 19 populations of Macrocystis pyrifera along its Eastern Pacific coastal distribution (EPC). The objective was to investigate the effects of male-female kinship on female fecundity and fertility, to estimate inbreeding depression in the F1 progeny, and to assess the variability of these effects among different regions and habitats of the EPC. Results revealed that the presence and kinship of males had a significant effect on fecundity and fertility of female gametophytes. Females left alone or in the presence of sibling males express the highest gametophyte size, number, and size of oogonia, suggesting they were able to sense the presence and the identity of their mates before gamete contact. The opposite trend was observed for the production of embryos per female gametes, indicating higher costs of selfing and parthenogenesis than outcrossing on fertility. However, the increased fecundity compensated for the reduced fertility, leading to a stable overall reproductive output. Inbreeding also affected morphological traits of juvenile sporophytes, but not their heatwave tolerance. The male-female kinship effect was stronger in high-latitude populations, suggesting that females from low-latitude marginal populations might have evolved to mate with any male gamete to guarantee reproductive success.