Limits...
Symbiosis limits establishment of legumes outside their native range at a global scale

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ABSTRACT

Microbial symbiosis is integral to plant growth and reproduction, but its contribution to global patterns of plant distribution is unknown. Legumes (Fabaceae) are a diverse and widely distributed plant family largely dependent on symbiosis with nitrogen-fixing rhizobia, which are acquired from soil after germination. This dependency is predicted to limit establishment in new geographic areas, owing to a disruption of compatible host-symbiont associations. Here we compare non-native establishment patterns of symbiotic and non-symbiotic legumes across over 3,500 species, covering multiple independent gains and losses of rhizobial symbiosis. We find that symbiotic legume species have spread to fewer non-native regions compared to non-symbiotic legumes, providing strong support for the hypothesis that lack of suitable symbionts or environmental conditions required for effective nitrogen-fixation are driving these global introduction patterns. These results highlight the importance of mutualisms in predicting non-native species establishment and the potential impacts of microbial biogeography on global plant distributions.

No MeSH data available.


Non-native ranges between symbiotic and non-symbiotic legumes species.(a) Mean number of introduced ranges across all legume species studied (including those with no introduced ranges) [(ntotal=180,030=(nspecies=3,530) × (nregions=51)]. (b) Mean number of introduced ranges for legume species recorded from at least one non-native region [(ntotal=41,412=(nspecies=812) × (nregions=51)]. A species' introduced range is defined by a list of geographic regions of non-native occurrence. Points and error bars represent the mean and 95% confidence intervals from parametric bootstraps, controlling for all covariates (absolute native latitude, total native area, life form, life history, area of non-native region and number of human uses).
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f2: Non-native ranges between symbiotic and non-symbiotic legumes species.(a) Mean number of introduced ranges across all legume species studied (including those with no introduced ranges) [(ntotal=180,030=(nspecies=3,530) × (nregions=51)]. (b) Mean number of introduced ranges for legume species recorded from at least one non-native region [(ntotal=41,412=(nspecies=812) × (nregions=51)]. A species' introduced range is defined by a list of geographic regions of non-native occurrence. Points and error bars represent the mean and 95% confidence intervals from parametric bootstraps, controlling for all covariates (absolute native latitude, total native area, life form, life history, area of non-native region and number of human uses).

Mentions: Within our dataset, 21.6% of all legume species occur in at least one non-native region (that is, polygon) and 15.8% occur in two or more non-native regions, confirming that many symbiotic and non-symbiotic legume species have successfully invaded or been introduced into new regions, continents and islands (Fig. 1). Our analysis of all species in the dataset at the regional level (see Methods section) show that symbiotic legumes have a significantly lower probability of occurring in non-native regions (Table 1), which translates into 49.7% fewer non-native regions per species (Fig. 2a). Furthermore, for successfully introduced species with at least one non-native range, we found that symbiotic legumes retain a lower probability of occurring in multiple non-native regions (Table 1), translating into 37.1% fewer numbers of non-native regions compared to non-symbiotic legumes (Fig. 2b). We excluded the possibility that non-native symbiotic legume species simply occurred in fewer yet much larger countries (Supplementary Note 1) by confirming that each non-symbiotic species had, on average, a larger total non-native range area (Supplementary Table 1) and no difference in the average size of individual regions that comprise the total introduced range area (Supplementary Table 1).


Symbiosis limits establishment of legumes outside their native range at a global scale
Non-native ranges between symbiotic and non-symbiotic legumes species.(a) Mean number of introduced ranges across all legume species studied (including those with no introduced ranges) [(ntotal=180,030=(nspecies=3,530) × (nregions=51)]. (b) Mean number of introduced ranges for legume species recorded from at least one non-native region [(ntotal=41,412=(nspecies=812) × (nregions=51)]. A species' introduced range is defined by a list of geographic regions of non-native occurrence. Points and error bars represent the mean and 95% confidence intervals from parametric bootstraps, controlling for all covariates (absolute native latitude, total native area, life form, life history, area of non-native region and number of human uses).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5385628&req=5

f2: Non-native ranges between symbiotic and non-symbiotic legumes species.(a) Mean number of introduced ranges across all legume species studied (including those with no introduced ranges) [(ntotal=180,030=(nspecies=3,530) × (nregions=51)]. (b) Mean number of introduced ranges for legume species recorded from at least one non-native region [(ntotal=41,412=(nspecies=812) × (nregions=51)]. A species' introduced range is defined by a list of geographic regions of non-native occurrence. Points and error bars represent the mean and 95% confidence intervals from parametric bootstraps, controlling for all covariates (absolute native latitude, total native area, life form, life history, area of non-native region and number of human uses).
Mentions: Within our dataset, 21.6% of all legume species occur in at least one non-native region (that is, polygon) and 15.8% occur in two or more non-native regions, confirming that many symbiotic and non-symbiotic legume species have successfully invaded or been introduced into new regions, continents and islands (Fig. 1). Our analysis of all species in the dataset at the regional level (see Methods section) show that symbiotic legumes have a significantly lower probability of occurring in non-native regions (Table 1), which translates into 49.7% fewer non-native regions per species (Fig. 2a). Furthermore, for successfully introduced species with at least one non-native range, we found that symbiotic legumes retain a lower probability of occurring in multiple non-native regions (Table 1), translating into 37.1% fewer numbers of non-native regions compared to non-symbiotic legumes (Fig. 2b). We excluded the possibility that non-native symbiotic legume species simply occurred in fewer yet much larger countries (Supplementary Note 1) by confirming that each non-symbiotic species had, on average, a larger total non-native range area (Supplementary Table 1) and no difference in the average size of individual regions that comprise the total introduced range area (Supplementary Table 1).

View Article: PubMed Central - PubMed

ABSTRACT

Microbial symbiosis is integral to plant growth and reproduction, but its contribution to global patterns of plant distribution is unknown. Legumes (Fabaceae) are a diverse and widely distributed plant family largely dependent on symbiosis with nitrogen-fixing rhizobia, which are acquired from soil after germination. This dependency is predicted to limit establishment in new geographic areas, owing to a disruption of compatible host-symbiont associations. Here we compare non-native establishment patterns of symbiotic and non-symbiotic legumes across over 3,500 species, covering multiple independent gains and losses of rhizobial symbiosis. We find that symbiotic legume species have spread to fewer non-native regions compared to non-symbiotic legumes, providing strong support for the hypothesis that lack of suitable symbionts or environmental conditions required for effective nitrogen-fixation are driving these global introduction patterns. These results highlight the importance of mutualisms in predicting non-native species establishment and the potential impacts of microbial biogeography on global plant distributions.

No MeSH data available.