Contrasting evolutionary histories from the warm Atlantic to the cold Pacific - overlooked seagrass diversity

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Seagrass connectivity on the West Coast of Africa supports the Hypothesis of Grazer-Mediated Seed Dispersal

Publication . Tavares, Ana I; Assis, Jorge; Patrício, A. R.; Ferreira, Rogério; Cheikh, Mohamed Ahmed Sidi; Bandeira, Salomão; Regalla, Aissa; Santos, Iderlindo; Potouroglou, Maria; Nicolau, Suzana; Teodosio, Maria; Almada, Carmen; Santos, Rui; Pearson, Gareth; Serrao, Ester

Population connectivity influences the distribution of genetic diversity and divergence along a species range, as the likelihood of extinction or differentiation increases in isolated populations. However, there is still poor understanding of the processes mediating inter-population dispersal in marine species that are sessile and lack planktonic life stages. One such case is the seagrass species Halodule wrightii, which produces basal seeds, although detached plants can drift. Along the tropical western coast of Africa, this species occurs in distant discontinuous habitats, raising the question of how interpopulation dispersal is mediated. The species is a key source of ecosystem functions including feeding large migratory grazers. This study aims to infer whether genetic differentiation of the seagrass H. wrightii along the western coast of Africa supports a hypothesis of predominant transportation of rafting seagrass by ocean currents, versus the hypothesis of biotic vectors of dispersal. Additional hypotheses were addressed concerning range-wide clonality and genetic diversity, assessed with microsatellite markers on populations of the west coast of Africa from Mauritania to Angola. Population genetic diversity and structure were compared with predictions from biophysical models of dispersal by oceanographic currents. The genetic data revealed low divergence among most populations, in strong contrast with predictions of very low probability of connectivity mediated by currents along the western African coastline. Moderate to high genotypic diversity showed important seed recruitment, but genetic and genotypic diversities were lower at range edges. Populations north and south of the equator were differentiated, and remarkably, so were neighboring equatorial populations despite their proximity. These results reveal independent sources of colonization of meadows in these islands, which are major habitat for migratory grazing green turtles, also supporting the hypothesis of biotically mediated seed transport. The importance of seagrass for conservation of endangered macrofauna has been widely reported; here we report evidence supporting the reciprocal role, that macrofauna protection can also plays a role in long-term survival and reproductive success of seagrass.

2022Journal article

Open access

Long range gene flow beyond predictions from oceanographic transport in a tropical marine foundation species

Publication . Tavares, Ana I; Assis, Jorge; Larkin, Patrick D.; Creed, Joel C.; Magalhães, Karine; Horta, Paulo; Engelen, Aschwin; Cardoso, Noelo; Barbosa, Castro; Pontes, Samuel; Regalla, Aissa; Almada, Carmen; Ferreira, Rogério; Abdoul, Ba Mamadou; Ebaye, Sidina; Bourweiss, Mohammed; dos Santos, Carmen Van-Dúnem; Patrício, Ana R.; Teodosio, Maria; Santos, Rui; Pearson, Gareth; Serrao, Ester A

The transport of passively dispersed organisms across tropical margins remains poorly understood. Hypotheses of oceanographic transportation potential lack testing with large scale empirical data. To address this gap, we used the seagrass species, Halodule wrightii, which is unique in spanning the entire tropical Atlantic. We tested the hypothesis that genetic differentiation estimated across its large-scale biogeographic range can be predicted by simulated oceanographic transport. The alternative hypothesis posits that dispersal is independent of ocean currents, such as transport by grazers. We compared empirical genetic estimates and modelled predictions of dispersal along the distribution of H. wrightii. We genotyped eight microsatellite loci on 19 populations distributed across Atlantic Africa, Gulf of Mexico, Caribbean, Brazil and developed a biophysical model with high-resolution ocean currents. Genetic data revealed low gene flow and highest differentiation between (1) the Gulf of Mexico and two other regions: (2) Caribbean-Brazil and (3) Atlantic Africa. These two were more genetically similar despite separation by an ocean. The biophysical model indicated low or no probability of passive dispersal among populations and did not match the empirical genetic data. The results support the alternative hypothesis of a role for active dispersal vectors like grazers.

2023-06Journal article

Open access

Contrasting evolutionary histories from the warm Atlantic to the cold Pacific - overlooked seagrass diversity

Publication . Tavares, Ana Isabel Magalhães; Serrão, Ester; Pearson, Gareth; Nakahoka, Masahiro

Marine connectivity and genetic differentiation among populations and species across different sides of oceans are hypothesized to be driven by contrasting processes in tropical versus cold and temperate regions. Tropical species occupy restricted warm ocean ranges where patterns of genetic differentiation might be driven more by oceanic connectivity and spatial habitat continuity and stepping stone processes. In contrast, the genetic structure across the ranges of species occupying cold and temperate habitats might be more influenced by the past climate-driven range shifts that led to demographic effects (e.g., bottlenecks, founder events, local extinctions, and expansions) with strong consequences for evolution and extant genetic diversity. There is well supported evidence for the role of Quaternary ice ages that had crucial effects on present distributions of species genetic diversity. Recurrent glacial-interglacial cycles led to a series of events shaping the phylogeographic patterns of marine species, leaving evidence that the present geographical genetic structure of northern hemisphere species has been strongly affected by historical vicariance. Seagrasses of the genera Halodule and Phyllospadix are distributed along coastal shores on both sides of the tropical Atlantic and temperate Pacific, respectively. They are therefore excellent models to study the impact of past and future climatic fluctuations and physical oceanographic connectivity on the patterns of genetic diversity and differentiation along the distributional ranges of both tropical and temperate regions. Additionally, these species they offer valuable insights into past range shifts and contemporary connectivity dynamics. This thesis aims to understand the population genetic history of seagrasses in biogeographical settings with contrasting oceanographic and seascape characteristics.

2024-02-22Doctoral thesis

Open access

Past and future climate effects on population structure and diversity of North Pacific surfgrasses

Publication . Tavares, Ana I; Assis, Jorge; Anderson, Laura; Raimondi, Pete; Coelho, Nelson; Paulino, Cristina; Ladah, Lydia; Nakaoka, Masahiro; Pearson, Gareth Anthony; Serrao, Ester A.

Understanding the impacts of past and future climate change on genetic diversity and structure is a current major research gap. We ask whether past range shifts explain the observed genetic diversity of surfgrass species and if future climate change projections anticipate genetic diversity losses. Our study aims to identify regions of long-term climate suitability with higher and unique seagrass genetic diversity and predict future impacts of climate change on them.LocationNortheast Pacific.Time PeriodAnalyses considered a timeframe from the Last Glacial Maximum (LGM; 20 kybp) until one Representative Concentration Pathway (RCP) scenario of future climate changes (RCP 8.5; 2100).Major Taxa StudiedTwo seagrass species belonging to the genus Phyllospadix.MethodsWe estimated population genetic diversity and structure using 11 polymorphic microsatellite markers. We predicted the distribution of the species for the present, LGM, and near future (RCP 8.5, no climate mitigation) using Species Distribution Models (SDMs).ResultsSDMs revealed southward range shifts during the LGM and potential poleward expansions in the future. Genetic diversity of Phyllospadix torreyi decreases from north to south, but in Phyllospadix scouleri the trend is variable. Phyllospadix scouleri displays signals of genome admixture at the southernmost and northernmost edges of its distribution.Main ConclusionsThe genetic patterns observed in the present reveal the influence of climate-driven range shifts in the past and suggest further consequences of climate change in the future, with potential loss of unique gene pools. This study also shows that investigating climate links to present genetic information at multiple timescales can establish a historical context for analyses of the future evolutionary history of populations.

2024-06-02Journal article

Open access