Evolutionary patterns of salt tolerance in angiosperms

Global food production is threatened by increasing land salinization triggered by climate change, land clearing, and irrigation. Salinity is toxic to most plants, including most crop species. A tremendous research effort has focused on understanding how a rare set of naturally salt tolerant plants, halophytes, are able to cope with soil salinity, as a model for producing salt tolerant crops. One largely unexplored area of research is the evolution of salt tolerance. Previous studies show that salt tolerance has evolved multiple times across the angiosperms, but little is known about the patterns and processes that underlie the evolution of salt tolerance. In my thesis I addressed several questions relating to the evolution of salt tolerance in angiosperms using a broad-scale, macroevolutionary approach. I first used taxonomic and phylogenetic comparative techniques to assess the evolutionary patterns of salt tolerance in angiosperms. I found that over one-third of angiosperm families contain halophytes and that salt tolerance appears to have evolved hundreds of times in the angiosperms. In over half of the family phylogenies analyzed, salt tolerance appeared evolutionarily labile: the origins of salt tolerance were scattered across phylogenies and generally gave rise to only one or a few halophytes. I also explored the association between salt tolerance and another trait associated with anthropogenic environmental change, heavy metal hyperaccumulation: the ability to accumulate high concentrations of heavy metals/metalloids. Taxonomic and physiological similarities suggest that salt tolerance may be associated with hyperaccumulation. I test the suggested relationship between these abilities using taxonomic and phylogenetic analyses. Significantly more angiosperm families contain both halophytes and hyperaccumulators and significantly more species are reported as both halophytes and hyperaccumulators than expected given the rarity of each trait. In several families, halophytes and hyperaccumulators are more closely related than expected if the two traits evolved independently. These results support the observation that salt tolerance and heavy metal hyperaccumulation are associated in angiosperms. Prolonged or repeated exposure to salinity can cause oxidative stress that may lead to increased mutation rates. These mutations may lead to increased substitution rates in halophytes compared to non-salt tolerant relatives. We tested this idea by comparing DNA sequences of multiple genes from the chloroplast, mitochondrial, and nuclear genomes from several halophytes with their non-salt tolerant relatives. We found that halophytes have significantly increased total substitution rates compared to their non-salt tolerant relatives in mitochondrial genes. This finding provides evidence that environmental factors may be associated with molecular rates. The goal of developing salt tolerant crops has proved incredibly difficult, which may be partly due to loss in genetic variation associated with domestication. Yet several studies suggest that domesticated animals and plants may have increased rates of molecular evolution, which could lead to increased variation. We test whether domesticates have consistently increased rates of molecular evolution by comparing the mitochondrial genomes of domesticated mammals and birds to their wild relatives. While a few domesticates exhibited higher rates, in general we found no consistent difference in mitochondrial rates of domesticated animals compared to their wild relatives. Keywords: comparative analysis, phylogenetics, domestication, macroevolution, rates of molecular evolution, halophyte

Salt tolerance is evolutionarily labile in a diverse set of angiosperm families

BACKGROUND: Salt tolerance in plants is rare, yet it is found across a diverse set of taxonomic groups. This suggests that, although salt tolerance often involves a set of complex traits, it has evolved many times independently in different angiosperm lineages. However, the pattern of evolution of salt tolerance can vary dramatically between families. A recent phylogenetic study of the Chenopodiaceae (goosefoot family) concluded that salt tolerance has a conserved evolutionary pattern, being gained early in the evolution of the lineage then retained by most species in the family. Conversely, a phylogenetic study of the Poaceae (grass family) suggested over 70 independent gains of salt tolerance, most giving rise to only one or a few salt tolerant species. Here, we use a phylogenetic approach to explore the macroevolutionary patterns of salt tolerance in a sample of angiosperm families, in order to ask whether either of these two patterns – deep and conserved or shallow and labile - represents a common mode of salt tolerance evolution. We analyze the distribution of halophyte species across the angiosperms and identify families with more or less halophytes than expected under a random model. Then, we explore the phylogenetic distribution of halophytes in 22 families using phylogenetic comparative methods. RESULTS: We find that salt tolerance species have been reported from over one-third of angiosperm families, but that salt tolerant species are not distributed evenly across angiosperm families. We find that salt tolerance has been gained hundreds of times over the history of the angiosperms. In a few families, we find deep and conserved gains of salt tolerance, but in the majority of families analyzed, we find that the pattern of salt tolerant species is best explained by multiple independent gains that occur near the tips of the phylogeny and often give rise to only one or a few halophytes. CONCLUSIONS: Our results suggest that the pattern of many independent gains of salt tolerance near the tips of the phylogeny is found in many angiosperm families. This suggests that the pattern reported in the grasses of high evolutionary lability may be a common feature of salt tolerance evolution in angiosperms

Data and analysis files for Domestication and the Mitochondrial Genome, Moray et al., GBE

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Data_salt_tolerance_angiosperms_Moray_et_al_BMC_Evo_Bio

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Prioritising in situ conservation of crop resources: A case study of African cowpea (Vigna unguiculata)

Conserving crop wild relatives (CWR) is critical for maintaining food security. However, CWR-focused conservation plans are lacking, and are often based on the entire genus, even though only a few taxa are useful for crop improvement. We used taxonomic and geographic prioritisation to identify the best locations for in situ conservation of the most important (priority) CWR, using African cowpea (Vigna unguiculata (L.) Walp.) as a case study. Cowpea is an important crop for subsistence farmers in sub-Saharan Africa, yet its CWR are under-collected, under-conserved and under-utilised in breeding. We identified the most efficient sites to focus in situ cowpea CWR conservation and assessed whether priority CWR would be adequately represented in a genus-based conservation plan. We also investigated whether priority cowpea CWR are likely to be found in existing conservation areas and in areas important for mammal conservation. The genus-based method captured most priority CWR, and the distributions of many priority CWR overlapped with established conservation reserves and targets. These results suggest that priority cowpea CWR can be conserved by building on conservation initiatives established for other species

Data from: Domestication and the mitochondrial genome: comparing patterns and rates of molecular evolution in domesticated mammals and birds and their wild relatives

Studies of domesticated animals have led to the suggestion that domestication could have significant effects on patterns of molecular evolution. In particular, analyses of mitochondrial genome sequences from domestic dogs and yaks have yielded higher ratios of non-synonymous to synonymous substitutions in the domesticated lineages than in their wild relatives. These results are important because they imply that changes to selection or population size operating over a short timescale can cause significant changes to the patterns of mitochondrial molecular evolution. In this study, our aim is to test whether the impact on mitochondrial genome evolution is a general feature of domestication, or whether it is specific to particular examples. We test whether domesticated mammals and birds have consistently different patterns of molecular evolution than their wild relatives for 16 phylogenetically independent comparisons of mitochondrial genome sequences. We find no consistent difference in branch lengths or dN/dS between domesticated and wild lineages. We also find no evidence that our failure to detect a consistent pattern is due to the short timescales involved, or low genetic distance between domesticated lineages and their wild relatives. However, removing comparisons where the wild relative may also have undergone a bottleneck does reveal a pattern consistent with reduced effective population size in domesticated lineages. Our results suggest that, while some domesticated lineages may have undergone changes to selective regime or effective population size that could have affected mitochondrial evolution, it is not possible to generalise these patterns over all domesticated mammals and birds

Data from: Salt tolerance is evolutionarily labile in a diverse set of angiosperm families

Background: Salt tolerance in plants is rare, yet they it is found across a diverse set of taxonomic groups. This suggests that, although salt tolerance involves a complex set of traits, it has evolved many times independently in different angiosperm lineages. However, the pattern of evolution of salt tolerance can vary dramatically between families. A recent phylogenetic study of the Chenopodiaceae (goosefoot family) concluded that salt tolerance has a conserved evolutionary pattern, being gained early in the evolution of the lineage then retained by most species in the family. Conversely, a phylogenetic study of the Poaceae (grass family) suggested over 70 independent origins of salt tolerance, most giving rise to only one or a few salt tolerant species. Here, we use a phylogenetic approach to explore the macroevolutionary patterns of salt tolerance in a sample of angiosperm families, in order to ask whether either of these two patterns - deep and conserved or shallow and labile - represents a common mode of salt tolerance evolution. We analyze the distribution of halophyte species across the angiosperms and identify families with more or less halophytes than expected under a random model. Then, we explore the phylogenetic distribution of halophytes in 22 families using phylogenetic comparative methods. Results: We find that salt tolerance species have been reported from over one-third of angiosperm families, but that salt tolerant species are not distributed evenly across angiosperm families. We find that salt tolerance has evolved hundreds of times over the history of the angiosperms. In a few families, we find deep and conserved origins of evolution of salt tolerance, but in the majority of families analyzed, we find that salt tolerance evolution is characterized by multiple independent origins that occur near the tips of the phylogeny and often give rise to only one or a few halophytes. Conclusions: Our results suggest that salt tolerance is evolutionarily labile in many different angiosperm families. Thus, the evolutionary pattern of many independent origins of salt tolerance near the tips of the phylogeny found previously in the grasses and observed in several other angiosperm families represents a common feature of salt tolerance evolution. Our findings add to the growing literature of the repeated evolution of complex ecological traits

The Phylogenetic Association Between Salt Tolerance and Heavy Metal Hyperaccumulation in Angiosperms**

Salt tolerance and heavy metal hyperaccumulation are two rare plant abilities that are heavily studied for their potential to contribute to agricultural sustainability and phytoremediation in response to anthropogenic environmental change. Several observations suggest that it is worth investigating the link between the abilities to tolerate high levels of soil salinity or accumulate more of a particular heavy metal from the soil than most plants. Firstly, several angiosperm families are known to contain both salt tolerant plants (halophytes) and heavy metal hyperaccumulators. Secondly, some halophytes can also accumulate heavy metals. Thirdly, although salinity tolerance and heavy metal hyperaccumulation typically require many physiological or anatomical changes, both have apparently evolved many times in angiosperms and among closely related species. We test for a significant relationship between halophytes and hyperaccumulators in angiosperms using taxonomic and phylogenetic analyses. We test whether there are more angiosperm families with both halophytes and hyperaccumulators than expected by chance, and whether there are more species identified as both halophyte and hyperaccumulator than if the abilities were unconnected. We also test whether halophytes and hyperaccumulators are phylogenetically clustered among species in seven angiosperm families. We find a significant association between halophytes and hyperaccumulators among angiosperm families and that there are significantly more species identified as both halophytes and hyperaccumulators than expected. Halophytes and hyperaccumulators each show low phylogenetic clustering, suggesting these abilities can vary among closely related species. In Asteraceae, Amaranthaceae, Fabaceae, and Poaceae, halophytes and hyperaccumulators are more closely related than if the two traits evolved independently

maternally inherited, lateralized trait pond snails is a Lymnaea stagnalis Mating behaviour in References Subject collections http://rsbl.royalsocietypublishing.org/subscriptions go to

Lateralization of the brain has traditionally been considered a specialization that is confined to the vertebrates, but recent studies have revealed that a range of invertebrates also have a brain that is structurally asymmetric and/or each side performs a different set of functions. Here, we show that the precopulatory mating behaviour of the pond snail Lymnaea stagnalis is lateralized. We present evidence that the asymmetry of the behaviour corresponds to the sinistral or dextral shell coil, or chirality, of the snail, and is apparently also controlled by a maternal effect locus. As sinistral snails also tend to have mirror image brains, these findings suggest that the lateralized sexual behaviour of L. stagnalis is set up early in development, and is a direct consequence of the asymmetry of the entire body