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- Sex-biased gene expression in the brown alga Fucus vesiculosusPublication . Martins, Maria João F.; Mota, Catarina; Pearson, G. A.Background The fucoid brown algae (Heterokontophyta, Phaeophyceae) are increasingly the focus of ecological genetics, biodiversity, biogeography and speciation research. The molecular genetics underlying mating system variation, where repeated dioecious – hermaphrodite switches during evolution are recognized, and the molecular evolution of sex-related genes are key questions currently hampered by a lack of genomic information. We therefore undertook a comparative analysis of male and female reproductive tissue transcriptomes against a vegetative background during natural reproductive cycles in Fucus vesiculosus. Results Over 300 k reads were assembled and annotated against public protein databases including a brown alga. Compared with the vegetative tissue, photosynthetic and carbohydrate metabolism pathways were under-expressed, particularly in male tissue, while several pathways involved in genetic information processing and replication were over-expressed. Estimates of sex-biased gene (SBG) expression were higher for male (14% of annotated orthologues) than female tissue (9%) relative to the vegetative background. Mean expression levels and variance were also greater in male- than female-biased genes. Major female-biased genes were carbohydrate-modifying enzymes with likely roles in zygote cell wall biogenesis and/or modification. Male-biased genes reflected distinct sperm development and function, and orthologues for signal perception (a phototropin), transduction (several kinases), and putatively flagella-localized proteins (including candidate gamete-recognition proteins) were uniquely expressed in males. Overall, the results suggest constraint on female-biased genes (possible pleiotropy), and less constrained male-biased genes, mostly associated with sperm-specific functions. Conclusions Our results support the growing contention that males possess a large array of genes regulating male fitness, broadly supporting findings in evolutionarily distant heterogametic animal models. This work identifies an annotated set of F. vesiculosus gene products that potentially regulate sexual reproduction and may contribute to prezygotic isolation, one essential step towards developing tools for a functional understanding of species isolation and differentiation.
- Driving south: a multi-gene phylogeny of the brown algal family Fucaceae reveals relationships and recent drivers of a marine radiationPublication . Cánovas, Fernando G.; Mota, Catarina; Serrão, Ester; Pearson, G. A.Understanding the processes driving speciation in marine ecosystems remained a challenge until recently, due to the unclear nature of dispersal boundaries. However, recent evidence for marine adaptive radiations and ecological speciation, as well as previously undetected patterns of cryptic speciation is overturning this view. Here, we use multi-gene phylogenetics to infer the family-level evolutionary history of Fucaceae (intertidal brown algae of the northern Pacific and Atlantic) in order to investigate recent and unique patterns of radiative speciation in the genus Fucus in the Atlantic, in contrast with the mainly monospecific extant genera. Results We developed a set of markers from 13 protein coding genes based on polymorphic cDNA from EST libraries, which provided novel resolution allowing estimation of ancestral character states and a detailed reconstruction of the recent radiative history. Phylogenetic reconstructions yielded similar topologies and revealed four independent trans-Arctic colonization events by Fucaceae lineages, two of which also involved transitions from hermaphroditism to dioecy associated with Atlantic invasions. More recently, reversion of dioecious ancestral lineages towards hermaphroditism has occurred in the genus Fucus, particularly coinciding with colonization of more extreme habitats. Novel lineages in the genus Fucus were also revealed in association with southern habitats. These most recent speciation events occurred during the Pleistocene glaciations and coincided with a shift towards selfing mating systems, generally southward shifts in distribution, and invasion of novel habitats. Conclusions Diversification of the family occurred in the Late-Mid Miocene, with at least four independent trans-Artic lineage crossings coincident with two reproductive mode transitions. The genus Fucus arose in the Pliocene but radiated within a relatively short time frame about 2.5 million years ago. Current species distributions of Fucus suggest that climatic factors promoted differentiation between the two major clades, while the recent and rapid species radiation in the temperate clade during Pleistocene glacial cycles coincided with several potential speciation drivers.
- Development and characterization of 35 single nucleotide polymorphism markers for the brown alga Fucus vesiculosusPublication . Cánovas, Fernando G.; Mota, Catarina; Ferreira Costa, J.; Serrão, Ester; Coyer, J. A.; Olsen, J. L.; Pearson, G. A.We characterized 35 single nucleotide polymorphism (SNP) markers for the brown alga Fucus vesiculosus. Based on existing Fucus Expressed Sequence Tag libraries for heat and desiccation-stressed tissue, SNPs were developed and confirmed by re-sequencing cDNA from a diverse panel of individuals. SNP loci were genotyped using the SEQUENOM single base extension iPLEXTM system for multiplex assays on the MassARRAY platform, which uses matrix-assisted laser desorption/ ionization time-of-flight mass spectrometry (MALDI-TOF MS) to discriminate allele-specific products. The SNP markers showed a wide range of variability among 16 populations from the south-west of the UK, northern Portugal and Morocco. The analysis of the information provided by these markers will be useful for studying population structure, historical demography and phylogeography of F. vesiculosus. They can also be used for the identification of genes and/or linked genomic regions potentially subject to selection in response to abiotic stressors like temperature extremes and desiccation intensity that vary across habitats and geographical range.
- Frayed at the edges: selective pressure and adaptive response to abiotic stressors are mismatched in low diversity edge populationsPublication . Pearson, Gareth; Lago-Lestón, Asunción; Mota, CatarinaTheory predicts that population structure and dynamics affect a population's capacity for adaptation to environmental change. For isolated, small and fragmented populations at the trailing edge of species distributions, loss of genetic diversity through random genetic drift may reduce adaptive potential and fitness levels for complex traits. This has important consequences for understanding population responses to, for example changing climate, but has rarely been tested in natural populations. We measured the intertidal thermal environment and tidal exposure (emersion) times for natural populations of the intertidal seaweed Fucus serratus at the centre (southwest UK) and southern edge (northern Portugal) of its range in the Eastern Atlantic, and for a congener, F. vesiculosus, whose range extends further south to Morocco. Fitness-related traits of individuals at each location were measured in common garden experiments: physiological resilience to desiccation and heat shock (PSII quantum yield), and the molecular phenotype of the heat shock response (quantitative PCR of heat shock protein gene transcripts). The realized thermal environment experienced by F. serratus was similar at the centre and southern edge of its distribution because the maximum shore height (and emersion period) was reduced in southern populations. For F. vesiculosus, thermal maxima were higher and occurred more frequently in the south, although maximum vertical height (emersion time) remained similar to central populations. Edge populations of F. serratus were less resilient to desiccation and heat shock than central populations, and expression of heat shock genes was higher at the same temperature, suggesting greater cellular stress. In contrast, there was no evidence for physiological divergence in heat shock response in F. vesiculosus, and little variation in gene expression. Synthesis. We provide evidence that compared with range-centre populations upper intertidal limits of F. serratus at the southern edge are 'pruned back' by abiotic stressors. Rather than being locally adapted, these small populations are less resilient to abiotic stresses and experience greater cellular stress during heat shock. These results suggest that ongoing climate forcing factors may threaten small, fragmented rear edge populations because of inherently reduced fitness and lower adaptive capacity relative to larger central populations.
- Differentiation in fitness-related traits in response to elevated temperatures between leading and trailing edge populations of marine macrophytesPublication . Mota, Catarina; Engelen, Aschwin; Serrao, Ester; Coelho, Márcio; Marba, Nuria; Krause-Jensen, Dorte; Pearson, GarethThe nature of species distribution boundaries is a key subject in ecology and evolution. Edge populations are potentially more exposed to climate-related environmental pressures. Despite research efforts, little is known about variability in fitness-related traits in leading (i.e., colder, high latitude) versus trailing (i.e., warmer, low latitude) edge populations. We tested whether the resilience, i.e. the resistance and recovery, of key traits differs between a distributional cold (Greenland) and warm (Portugal) range edge population of two foundation marine macrophytes, the intertidal macroalga Fucus vesiculosus and the subtidal seagrass Zostera marina. The resistance and recovery of edge populations to elevated seawater temperatures was compared under common experimental conditions using photosynthetic efficiency and expression of heat shock proteins (HSP). Cold and warm edge populations differed in their response, but this was species specific. The warm edge population of F. vesiculosus showed higher thermal resistance and recovery whereas the cold leading edge was less tolerant. The opposite was observed in Z. marina, with reduced recovery at the warm edge, while the cold edge was not markedly affected by warming. Our results confirm that differentiation of thermal stress responses can occur between leading and trailing edges, but such responses depend on local population traits and are thus not predictable just based on thermal pressures.
- Some don't like it hot: microhabitat-dependent thermal and water stresses in a trailing edge populationPublication . Mota, Catarina F.; Engelen, Aschwin H.; Serrao, Ester A.; Pearson, Gareth A.The distributional limits of species in response to environmental change are usually studied at large temporal and/or geographical scales. However, organismal scale habitat variation can be overlooked when investigating large-scale averages of key factors such as temperature. We examine how microhabitat thermal conditions relate to physiological limits, which may contribute to recent range shifts in an intertidal alga. We defined the onset and maximum temperatures of the heat-shock response (HSR) for a southern edge population of Fucus vesiculosus, which has subsequently become extinct. The physiological threshold for resilience (assayed using chlorophyll fluorescence) coincided with declining HSR, determined from the temperature-dependent induction of seven heat-shock protein transcripts. In intertidal habitats, temperature affects physiology directly by controlling body temperature and indirectly through evaporative water loss. We investigated the relationship between the thermal environment and in situ molecular HSR at microhabitat scales. Over cm to m scales, four distinct microhabitats were defined in algal patches (canopy surface, patch edge, subcanopy, submerged channels), revealing distinct thermal and water stress environments during low-tide emersion. The in situ HSR agreed with estimated tissue temperatures in all but one microhabitat. Remarkably, in the most thermally extreme microhabitat (canopy surface), the HSR was essentially absent in desiccated tissue, providing a potential escape from the cellular metabolic costs of thermal stress. Meteorological records, microenvironmental thermal profiles and HSR data indicate that the maximum HSR is approached or exceeded in hydrated tissue during daytime low tides for much of the year. Furthermore, present-day summer seawater temperatures are sufficient to induce HSR during high-tide immersion, preventing recovery and resulting in continuous HSR during daytime low-tide cycles over the entire summer. HSR in the field matched microhabitat temperatures more closely than local seawater or atmospheric data, suggesting that the impacts of climatic change are best understood at the microhabitat scale, particularly in intertidal areas.