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- Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structurePublication . I Zardi, Gerardo; Nicastro, Katy R; Ferreira Costa, J.; Serrão, Ester; Pearson, G. A.Understanding the extent to which neutral processes and adaptive divergence shape the spatial structure of natural populations is a major goal in evolutionary biology and is especially important for the identification of significant levels of biodiversity. Our results identified replicated habitat-specific (adaptive) phenotypic divergence in the brown macroalga Fucus vesiculosus that is independent of population (neutral) genetic structure. F. vesiculosus inhabits contiguous and contrasting marine to estuarine intertidal habitats. Combining analyses of genetic and phenotypic traits of populations living under differential selective regimes (estuaries and open coast), we investigated levels of neutral genetic differentiation and adaptive physiological responses to emersion stress. In southwest England (SW UK) and northern Iberia (N. Iberia), populations living in estuaries and marine coastal habitats were genetically characterized at six microsatellite loci. In N. Iberia, two clades with limited admixture were recovered, each including one open coast site and the adjacent estuarine location. In contrast, SW UK samples clustered according to habitat and formed three distinct groups of genotypes; one including the two open coast locations and the other two representing each of the estuarine sites. Temperature loggers revealed distinct emersion regimes that characterized each habitat type independently of the region, while water and air temperature profiles showed site-specific trends. Despite acclimation under usual conditions, trait means of emersion stress resilience showed a strong phenotypic divergence between habitats, consistent with environmental clines in exposure time observed in the different habitats. We demonstrate that neutral genetic clusters do not reflect locally adapted population units. Our results identified replicated habitat-specific (adaptive) phenotypic divergence that is independent of population (neutral) genetic structure in F. vesiculosus. The significance of such findings extends beyond the theoretical evolutionary and ecological interest of discovering parallel adaptive responses to the broader implications for conservation of intraspecific biodiversity.
- Coastal topography drives genetic structure in marine musselsPublication . Nicastro, Katy; Zardi, Gerardo; McQuaid, C. D.; Teske, P. R.; Barker, N. P.Understanding population connectivity is fundamental] to ecology, and, for sedentary organisms, connectivity is achieved through larval dispersal. We tested whether coastal topography influences genetic structure in Perna Perna mussels by comparing populations inside bays and on the open coast. Higher hydrodynamic stress on the open coast produces higher mortality and thus genetic turnover. Populations on the open coast had fewer private haplotypes and less genetic endemism than those inside bays. Gene flow analysis showed that bays act as Source populations, with greater migration rates Out. of bays than into them. Differences in genetic structure on scales of 10s of kilometres show that coastal configuration strongly affects selection, larval dispersal and haplotype diversity,
- Love thy neighbour: group properties of gaping behaviour in mussel aggregationsPublication . Nicastro, Katy R; I Zardi, Gerardo; McQuaid, C. D.; Pearson, G. A.; Serrão, EsterBy associating closely with others to form a group, an animal can benefit from a number of advantages including reduced risk of predation, amelioration of environmental conditions, and increased reproductive success, but at the price of reduced resources. Although made up of individual members, an aggregation often displays novel effects that do not manifest at the level of the individual organism. Here we show that very simple behaviour in intertidal mussels shows new effects in dense aggregations but not in isolated individuals. Perna perna and Mytilus galloprovincialis are gaping (periodic valve movement during emersion) and non-gaping mussels respectively. P. perna gaping behaviour had no effect on body temperatures of isolated individuals, while it led to increased humidity and decreased temperatures in dense groups (beds). Gaping resulted in cooler body temperatures for P. perna than M. galloprovincialis when in aggregations, while solitary individuals exhibited the highest temperatures. Gradients of increasing body temperature were detected from the center to edges of beds, but M. galloprovincialis at the edge had the same temperature as isolated individuals. Furthermore, a field study showed that during periods of severe heat stress, mortality rates of mussels within beds of the gaping P. perna were lower than those of isolated individuals or within beds of M. galloprovincialis, highlighting the determinant role of gaping on fitness and group functioning. We demonstrate that new effects of very simple individual behaviour lead to amelioration of abiotic conditions at the aggregation level and that these effects increase mussel resistance to thermal stress.
- Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosusPublication . Nicastro, Katy R; I Zardi, Gerardo; Teixeira, Sara; Neiva, J.; Serrão, Ester; Pearson, G. A.Significant effects of recent global climate change have already been observed in a variety of ecosystems, with evidence for shifts in species ranges, but rarely have such consequences been related to the changes in the species genetic pool. The stretch of Atlantic coast between North Africa and North Iberia is ideal for studying the relationship between species distribution and climate change as it includes the distributional limits of a considerable number of both cold- and warm-water species. We compared temporal changes in distribution of the canopy-forming alga Fucus vesiculosus with historical sea surface temperature (SST) patterns to draw links between range shifts and contemporary climate change. Moreover, we genetically characterized with microsatellite markers previously sampled extinct and extant populations in order to estimate resulting cryptic genetic erosion. Results Over the past 30 years, a geographic contraction of the southern range edge of this species has occurred, with a northward latitudinal shift of approximately 1,250 km. Additionally, a more restricted distributional decline was recorded in the Bay of Biscay. Coastal SST warming data over the last three decades revealed a significant increase in temperature along most of the studied coastline, averaging 0.214°C/decade. Importantly, the analysis of existing and extinct population samples clearly distinguished two genetically different groups, a northern and a southern clade. Because of the range contraction, the southern group is currently represented by very few extant populations. This southern edge range shift is thus causing the loss of a distinct component of the species genetic background. Conclusions We reveal a climate-correlated diversity loss below the species level, a process that could render the species more vulnerable to future environmental changes and affect its evolutionary potential. This is a remarkable case of genetic uniqueness of a vanishing cryptic genetic clade (southern clade).
- Intraspecific genetic lineages of a marine mussel show behavioural divergence when exposed to microplastic leachatesPublication . Cozzolino, Lorenzo; Nicastro, Katy R; Hubbard, Peter; Seuront, Laurent; McQuaid, Christopher D.; Zardi, Gerardo IWorldwide, microplastic pollution has numerous negative implications for marine biota, exacerbating the effects of other forms of global anthropogenic disturbance. Mounting evidence shows that microplastics (MPs) not only cause physical damage through their ingestion, but also act as vectors for hazardous compounds by leaching absorbed and adsorbed chemicals. Research on the effects of plastic pollution has, however, largely assumed that species respond uniformly, while ignoring intraspecific diversity (i.e., variation within a single species). We investigated the effects of plastic leachates derived from factory-fresh (virgin) and beached microplastics on the behavioural responses of two genetic lineages of the Mediterranean mussel Mytilus galloprovincialis. Through laboratory behavioural experiments, we found that during exposure to leachates from beached microplastics (beached MPLs), Atlantic specimens moved significantly less than Mediterranean individuals in terms of both (i) proportion of individuals responding through movement and (ii) net and gross distances crawled. In contrast, no significant intraspecific differences were observed in the behaviour of either adults or recruits when exposed to MPLs from virgin microplastics (virgin MPLs). Additionally, the reception of cues from three amino acids (Lcysteine, proline and L-leucine) at increasing concentrations (10-5 M to 10-3 M in charcoal-filtered seawater) was tested by electrophysiological analysis using mussels exposed to beached MPLs or control seawater. We found significant intraspecific differences in response to 10-3 M L-cysteine (regardless of treatment) and 10-4 M L-cysteine (in mussels exposed to beached MPLs) and to 10-3 M proline (in mussels exposed to beached MPLs) and 10-5 M L-leucine. Our study suggests that intraspecific variation in a marine mussel may prompt different responses to plastic pollution, potentially triggered by local adaptation and physiological variability between lineages. Our work highlights the importance of assessing the effects of intraspecific variation, especially in environmental sentinel species as this level of diversity could modulate responses to plastic pollution.
- Effects of endolithic parasitism on invasive and indigenous mussels in a Variable Physical EnvironmentPublication . I Zardi, Gerardo; Nicastro, Katy; McQuaid, Christopher David; Gektidis, MarcosBiotic stress may operate in concert with physical environmental conditions to limit or facilitate invasion processes while altering competitive interactions between invaders and native species. Here, we examine how endolithic parasitism of an invasive and an indigenous mussel species acts in synergy with abiotic conditions of the habitat. Our results show that the invasive Mytilus galloprovincialis is more infested than the native Perna perna and this difference is probably due to the greater thickness of the protective outer-layer of the shell of the indigenous species. Higher abrasion due to waves on the open coast could account for dissimilarities in degree of infestation between bays and the more wave-exposed open coast. Also micro-scale variations of light affected the level of endolithic parasitism, which was more intense at non-shaded sites. The higher levels of endolithic parasitism in Mytilus mirrored greater mortality rates attributed to parasitism in this species. Condition index, attachment strength and shell strength of both species were negatively affected by the parasites suggesting an energy trade-off between the need to repair the damaged shell and the other physiological parameters. We suggest that, because it has a lower attachment strength and a thinner shell, the invasiveness of M. galloprovincialis will be limited at sun and wave exposed locations where endolithic activity, shell scouring and risk of dislodgement are high. These results underline the crucial role of physical environment in regulating biotic stress, and how these physical-biological interactions may explain site-to-site variability of competitive balances between invasive and indigenous species.
- Microplastic leachates inhibit small-scale self-organization in mussel bedsPublication . Zardi, Gerardo I; Nicastro, Katy R; Truong, Stéphanie Lau; Decorse, Philippe; Nozak, Sophie; Chevillot-Biraud, Alexandre; Froneman, Pierre William; Akoueson, Fleurine; Duflos, Guillaume; Seuront, LaurentSelf-organized spatial patterns are increasingly recognized for their contribution to ecosystem functioning. They can improve the ecosystem's ability to respond to perturbation and thus increase its resilience to environmental stress. Plastic pollution has now emerged as major threat to aquatic and terrestrial biota. Under laboratory conditions, we tested whether plastic leachates from pellets collected in the intertidal can impair small-scale, spatial self-organization and byssal threads production of intertidal mussels and whether the effect varied depending on where the pellets come from. Specifically, leachates originating from plastic pellets collected from relatively pristine and polluted areas respectively impaired and inhibited the ability of mussels to self-organize at small-scale and to produce byssal threads compared to control conditions (i.e., seawater without leaching solution). Limitations to natural self-organizing processes and threads formation may translate to a declined capacity of natural ecosystems to avoid tipping points and to a reduced restoration success of disturbed ecosystems.
- First record of the brown mussel (Perna perna) from the European Atlantic coastPublication . Lourenço, Carla R.; Nicastro, Katy R; Serrão, Ester; I Zardi, GerardoThe occurrence of the brown mussel Perna perna is reported for the first time from the European Atlantic coast, on the southern Portuguese coast. Several specimens of this mytilidae species were identified in exposed rocky intertidal habitats in Vilamoura (37804019.7000N 8807019.7100W) and Ilha do Farol (36858029.3800N 7851042.5100W). It is suggested that, under warming climate conditions, this subtropical/tropical species might have extended its geographical distribution from North Africa.
- Characterization of ten highly polymorphic microsatellite loci for the intertidal mussel Perna perna, and cross species amplification within the genusPublication . Coelho, Nelson; I Zardi, Gerardo; Pearson, G. A.; Serrão, Ester; Nicastro, Katy RThe brown mussel Perna perna (Linnaeus, 1758) is a dominant constituent of intertidal communities and a strong invader with multiple non-native populations distributed around the world. In a previous study, two polymorphic microsatellite loci were developed and used to determine population-level genetic diversity in invasive and native P. perna populations. However, higher number of microsatellite markers are required for reliable population genetic studies. In this context, in order to understand P. perna origins and history of invasion and to compare population genetic structure in native versus invaded areas, we developed 10 polymorphic microsatellite markers. Findings Described microsatellite markers were developed from an enriched genomic library. Analyses and characterization of loci using 20 individuals from a population in Western Sahara revealed on average 11 alleles per locus (range: 5–27) and mean gene diversity of 0.75 (range: 0.31 - 0.95). One primer pair revealed possible linkage disequilibrium while heterozygote deficiency was significant at four loci. Six of these markers cross-amplified in P. canaliculus (origin: New Zealand). Conclusions Developed markers will be useful in addressing a variety of questions concerning P. perna, including dispersal scales, genetic variation and population structure, in both native and invaded areas.
- Movement behaviour and mortality in invasive and indigenous mussels: resilience and resistance strategies at different spatial scalesPublication . Nicastro, Katy; Zardi, Gerardo; McQuaid, C. D.The responses of indigenous and exotic species to environmental factors can differ across spatial and temporal scales, and it is this difference that determines invasion success and the dynamics of co-existence, In South Africa, the indigenous Perna perna and the invasive Mytilus galloprovincialis are the dominant intertidal mussels on the southern coast, where they co-exist. We compared their movement behaviour over 6 mo at small scales (within and at the edge of mussel beds) and at meso scales (in bays and on the open coast). M, galloprovincialis moved more and had higher mortality rates than did P. perna. For both species, mortality was greater at the edge than at the centre of beds, and on the open coast than in bays. Mussels at the edge of beds moved more than those within beds, but, while this was true for M. galloprovincialis in both habitats, P. perna did not show a position effect on the open coast. Cross-correlation analysis showed that movement rates of both species were correlated with mortality rates after a lag of 1. mo. These results suggest that following mortality events, mussels react to increased availability of space and decreased attachment to neighbours by increasing their movement to reorganise into a safer arrangement. However, P. perna and M. galloprovincialis effectively adopt resistance and resilience strategies, respectively. The effectiveness of each strategy depends on environmental conditions in different habitats, influencing the possibility of co-existence. The higher hydrodynamic stresses experienced in open coast habitats and at the edge of a mussel bed are disadvantageous to the more active, less strongly attached invasive species.