Restoration genetics of north-west European saltmarshes: A multi-scale analysis of population genetic structure in Puccinellia maritima and Triglochin maritima

Increasing human pressure combined with sea level rise and increased storminess is threatening coastal ecosystems around the world. Among these ecosystems, saltmarshes are particularly endangered due to their position in temperate areas with low wave action where human density is often high (e.g. estuaries). Around the UK, centuries of land reclamation have led to a substantial decrease of the area of saltmarsh. Over the past decades, restoration schemes have been implemented in numerous coastal locations in an attempt to counteract this loss. Such schemes involve allowing sea water to inundate a previously embanked area and letting the vegetation develop naturally, thereby reverting to saltmarsh through natural colonisation. However, surveys of restored areas that have looked at the recovery of plant species diversity or functional characteristics often show that restored saltmarshes do not reach the state of a natural saltmarsh ecosystem. While there is much data at the species level, recovery of plant intra-specific diversity (genetic diversity) has not been assessed in restored saltmarsh although this component of biodiversity is receiving increasing attention for its effect on ecosystem function. This thesis represents the first attempt to (1) characterize the nation-wide genetic structure of two important north-west European saltmarsh plant species, the common saltmarsh grass (Puccinellia maritima) and the sea arrowgrass (Triglochin maritima) and (2) compare levels of genetic diversity and structure between restored and natural ecosystems. Microsatellite molecular markers were developed for both species. Using innovative methods to analyse the genetic data obtained for these two polyploid species, this thesis highlights that genetic diversity at the national scale is organised regionally for both species, although gene-flow is still restricted between populations within the same region. Gene-flow between populations is determined by different processes depending on the species. While coastal processes mainly influence gene dispersal in P. maritima, overland routes of dispersal are involved for T. maritima. These differences are believed to be due to differences in dispersal ecology between the two species. Although gene-flow exists between distant saltmarshes, the genetic analysis of P. maritima and T. maritima colonists arriving on restored sites highlighted their local origin and reaffirmed that it is preferable to restore saltmarsh where a nearby natural saltmarsh can act as a source of colonists. A multiple paired-site comparison identified similar genetic diversity between restored and natural saltmarshes indicating that restoration of local genetic diversity is rapid for both species. A single site comparison at Skinflats in the Forth estuary compared fine-scale spatial genetic structure between the restored and natural saltmarsh. Interestingly, no structure was detected for T. maritima either in restored or natural saltmarsh. In contrast, a strong genetic structure organised along the elevation gradient was observed in the natural saltmarsh for P. maritima but was absent in the restored saltmarsh. The origin of this structure is not clear but could be due to restricted gene-flow between individuals from different elevations due to strong post-zygotic selection, as suggested in previous work. In any case, this lack of structure in the restored saltmarsh indicates that genetic recovery is incomplete in this respect for P. maritima. This thesis introduces the growing field of restoration genetics to saltmarsh ecology and identifies the principal population genetic trends in two of the species dominating the vegetation of north-west European saltmarshes community. The information given here will be useful for restoration practitioners and provides a strong foundation for future work characterizing the importance of genetic diversity for saltmarsh function

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A seascape genetic analysis reveals strong biogeographical structuring driven by contrasting processes in the polyploid saltmarsh species Puccinellia maritima and Triglochin maritima

Little is known about the processes shaping population structure in saltmarshes. It is expected that the sea should act as a powerful agent of dispersal. Yet, in contrast, import of external propagules into a saltmarsh is thought to be small. To determine the level of connectivity between saltmarsh ecosystems at a macro-geographical scale, we characterized and compared the population structure of two polyploid saltmarsh species, Puccinellia maritima and Triglochin maritima based on a seascape genetics approach. A discriminant analysis of principal components highlighted a genetic structure for both species arranged according to a regional pattern. Subsequent analysis based on isolation-by-distance and isolation-by-resistance frameworks indicated a strong role of coastal sediment transport processes in delimiting regional structure in P. maritima, while additional overland propagule dispersal was indicated for T. maritima. The identification and comparison of regional genetic structure and likely determining factors presented here allows us to understand the biogeographical units along the UK coast, between which barriers to connectivity occur not only at the species level but at the ecosystem scale. This information is valuable in plant conservation and community ecology and in the management and restoration of saltmarsh ecosystems

Fine-scale spatial genetic structure across a strong environmental gradient in the saltmarsh plant Puccinellia maritima

Saltmarsh forms the transition between maritime and terrestrial environments where biotic and abiotic conditions vary substantially along a gradient in elevation. Theoretical and empirical population genetics studies have focused on the influence of environmental gradients on intra-specific genetic variation. Contrastingly, only a few studies have focused on genetic variation in saltmarsh plants, despite the potentially strong influence of environmental gradients shaping diversity in these species. In the present paper, we assess the genetic structure of the saltmarsh plant Puccinellia maritima collected across an elevation gradient in restored and natural saltmarsh. Both spatial autocorrelograms of genetic variation and spatial analysis of principal components detected genetic structurein the natural saltmarsh organized along the gradient in elevation, yet no such pattern was identified considering distance between individuals without taking elevation into account. In combination with previous phenotypic analyses, our results imply that ecological divergence likely plays a key role in shaping genetic structure within saltmarsh species. Comparison of restored and natural saltmarsh indicated that interspecific competition plays an important role in shaping the genetic structure observed on the natural saltmarsh. The results of this study demonstrate that saltmarshes are valuable models in which to test effects of ecological differentiation and, by extension, provide a better understanding of the functioning of this threatened environment

Pairwise effective resistance between Triglochin maritima population (TIDE_SEDCELLS model)

Matrix of pairwise effective resistance (TIDE_SEDCELLS model) between Triglochin maritima population inferred using the software Circuitscape. This matrix is inputted in R for Mantel test

Puccinellia maritima DAPC script

R script permitting to compute DAPC for Puccinellia maritim

Triglochin maritima population assignment to DAPC regions (K=4)

Triglochin maritima input file for the implementation of the AMOV

Mantel test script

R script permitting to compute Mantel test

Pairwise effective resistance between Puccinellia maritima population (SEDCELLS model)

Matrix of pairwise effective resistance (SEDCELLS model) between Puccinellia maritima population inferred using the software Circuitscape. This matrix is inputted in R for Mantel test

Pairwise effective resistance between Puccinellia maritima population (TIDE model)

Matrix of pairwise effective resistance (TIDE model) between Puccinellia maritima population inferred using the software Circuitscape. This matrix is inputted in R for Mantel test