skip to main content


Title: Is the central‐marginal hypothesis a general rule? Evidence from three distributions of an expanding mangrove species, Avicennia germinans (L.) L
Abstract

The central‐marginal hypothesis (CMH) posits that range margins exhibit less genetic diversity and greater inter‐population genetic differentiation compared to range cores. CMH predictions are based on long‐held “abundant‐centre” assumptions of a decline in ecological conditions and abundances towards range margins. Although much empirical research has confirmed CMH, exceptions remain almost as common. We contend that mangroves provide a model system to test CMH that alleviates common confounding factors and may help clarify this lack of consensus. Here, we document changes in black mangrove (Avicennia germinans) population genetics with 12 nuclear microsatellite loci along three replicate coastlines in the United States (only two of three conform to underlying “abundant‐centre” assumptions). We then test an implicit prediction of CMH (reduced genetic diversity may constrain adaptation at range margins) by measuring functional traits of leaves associated with cold tolerance, the climatic factor that controls these mangrove distributional limits. CMH predictions were confirmed only along the coastlines that conform to “abundant‐centre” assumptions and, in contrast to theory, range marginA. germinansexhibited functional traits consistent with greater cold tolerance compared to range cores. These findings support previous accounts that CMH may not be a general rule across species and that reduced neutral genetic diversity at range margins may not be a constraint to shifts in functional trait variation along climatic gradients.

 
more » « less
NSF-PAR ID:
10375654
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Molecular Ecology
Volume:
29
Issue:
4
ISSN:
0962-1083
Page Range / eLocation ID:
p. 704-719
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Due to a warming climate, mangrove populations within the Gulf of Mexico and along the Florida Atlantic coastline are expanding their range poleward. As mangroves expand their range limit, leading edge individuals are more likely to experience an increased incidence of freeze events. However, we still lack a clear understanding of the mechanisms used by mangroves to survive freezing conditions.

    Here, we conducted common garden experiments at different locations experiencing variable winter freeze conditions to show glycine betaine, an organic osmolyte, increases significantly with freeze exposure, playing an important role in the freeze tolerance ofAvicennia germinans, a widespread Neotropical mangrove.

    We found glycine betaine accumulation was similar across all source populations and freeze exposure locations, suggesting glycine betaine is not a range limit adaptation and is instead used for freeze tolerance byA. germinansirrespective of source population. Plants sourced from populations that experience freezing conditions exhibited greater rates of survival, indicating range edge populations ofA. germinanshave other heritable adaptations in addition to glycine betaine for freeze tolerance.

    Synthesis. Continued mangrove expansion poleward will result in a greater incidence of freeze events for individuals at the leading edge. Our findings suggest freeze tolerance in this species may be genetically based and that leading edgeA. germinanshave the potential to survive extreme freeze events and recover post‐freeze, allowing for their continued expansion poleward. This process of selective survival may act to promote adaptation of freeze tolerance in range edge populations.

     
    more » « less
  2. Abstract

    Increases in minimum air temperatures have facilitated transitions of salt marshes to mangroves along coastlines in the southeastern United States. Numerous studies have documented mangrove expansion into salt marshes; however, a present‐day conversion of oyster reefs to mangrove islands has not been documented. Using aerial photographs and high‐resolution satellite imagery, we determined percent cover and number of mangrove patches on oyster reefs in Mosquito Lagoon, FL, USA over 74 years (1943–2017) by digitizing oyster reef and “mangrove on oyster reef” areas. Live oyster reefs present in 1943 were tracked through time and the mangrove area on every reef calculated for seven time periods. There was a 103% increase in mangrove cover on live oyster reefs from 1943 (6.6%) to 2017 (13.4%). Between 1943 and 1984, the cover remained consistent (~7%), while between 1984 and 2017, mangrove cover increased rapidly with a 6% year−1increase in mangrove area on oyster reefs (198% increase). In 1943, 8.7% of individual reefs had at least one mangrove patch on them; by 2017, 21.8% of reefs did. Site visits found at least one matureAvicennia germinanson each tracked mangrove reef, with large numbers of smallerRhizophora mangle, suggesting the post‐1984 mangrove increases were the result of increasedR. manglerecruitment and survival. Escalation in the coverage and number of mangrove stands on oyster reefs coincided with a period that lacked extreme freeze events. The time since a temperature of ≤−6.6°C (A.germinansmortality threshold) and ≤−4°C (R. manglemortality threshold) were significantly correlated with the increased ratio of mangrove area:oyster area, total mangrove area, and number of mangrove patches, with greater variation explained by time since ≤ −4°C. The lack of freezes could lead globally to an ecosystem shift of intertidal oyster reefs to mangrove islands near poleward mangrove range limits.

     
    more » « less
  3. Abstract

    A lack of optimal gene combinations, as well as low levels of genetic diversity, is often associated with the formation of species range margins. Conservation efforts rely on predictive modelling using abiotic variables and assessments of genetic diversity to determine target species and populations for controlled breeding, germplasm conservation and assisted migration. Biotic factors such as interspecific competition and hybridization, however, are largely ignored, despite their prevalence across diverse taxa and their role as key evolutionary forces. Hybridization between species with well‐developed barriers to reproductive isolation often results in the production of offspring with lower fitness. Generation of novel allelic combinations through hybridization, however, can also generate positive fitness consequences. Despite this possibility, hybridization‐mediated introgression is often considered a threat to biodiversity as it can blur species boundaries. The contribution of hybridization towards increasing genetic diversity of populations at range margins has only recently gathered attention in conservation studies. We assessed the extent to which hybridization contributes towards range dynamics by tracking spatio‐temporal changes in the central location of a hybrid zone between two recently diverged species of pines:Pinus strobiformisandP. flexilis. By comparing geographic cline centre estimates for global admixture coefficient with morphological traits associated with reproductive output, we demonstrate a northward shift in the hybrid zone. Using a combination of spatially explicit, individual‐based simulations and linkage disequilibrium variance partitioning, we note a significant contribution of adaptive introgression towards this northward movement, despite the potential for differences in regional population size to aid hybrid zone movement. Overall, our study demonstrates that hybridization between recently diverged species can increase genetic diversity and generate novel allelic combinations. These novel combinations may allow range margin populations to track favourable climatic conditions or facilitate adaptive evolution to ongoing and future climate change.

     
    more » « less
  4. Abstract Aim

    Correlative distribution models have been used to identify potential climatic controls of mangrove range limits, but there is still uncertainty about the relative importance of these factors across different regions. To provide insights into the strength of climatic control of different mangrove range limits, we tested whether temporal variability in mangrove abundance increases near range limits and whether this variability is correlated with climatic factors thought to control large‐scale mangrove distributions.

    Location

    North and South America.

    Time period

    1984–2011.

    Major taxa studied

    Avicennia germinans,Avicennia schuaeriana,Rhizophora mangle,Laguncularia racemosa.

    Methods

    We characterized temporal variability in the enhanced vegetation index (EVI) at mangrove range limits using Landsat satellite imagery collected between 1984–2011. We characterized greening trends at each range limit, examined variability in EVI along latitudinal gradients near each range limit, and assessed correlations between changes in EVI and temperature and precipitation.

    Results

    Spatial variability in mean EVI was generally correlated with temperature and precipitation, but the relationships were region specific. Greening trends were most pronounced at range limits in eastern North America. In these regions variability in EVI increased toward the range limit and was sensitive to climatic factors. In contrast, EVI at range limits on the Pacific coast of North America and both coasts of South America was relatively stable and less sensitive to climatic variability.

    Main conclusions

    Our results suggest that range limits in eastern North America are strongly controlled by climate factors. Mangrove expansion in response to future warming is expected to be rapid in regions that are highly sensitive to climate variability (e.g. eastern North America), but the response in other range limits (e.g. South America) is likely to be more complex and modulated by additional factors such as dispersal limitation, habitat constraints, and/or changing climatic means rather than just extremes.

     
    more » « less
  5. Abstract

    Global change is widely altering environmental conditions which makes accurately predicting species range limits across natural landscapes critical for conservation and management decisions. If climate pressures along elevation gradients influence the distribution of phenotypic and genetic variation of plant functional traits, then such trait variation may be informative of the selective mechanisms and adaptations that help define climatic niche limits. Using extensive field surveys along 16 elevation transects and a large common garden experiment, we tested whether functional trait variation could predict the climatic niche of a widespread tree species (Populus angustifolia) with a double quantile regression approach. We show that intraspecific variation in plant size, growth, and leaf morphology corresponds with the species' total climate range and certain climatic limits related to temperature and moisture extremes. Moreover, we find evidence of genetic clines and phenotypic plasticity at environmental boundaries, which we use to create geographic predictions of trait variation and maximum values due to climatic constraints across the western US. Overall, our findings show the utility of double quantile regressions for connecting species distributions and climate gradients through trait‐based mechanisms. We highlight how new approaches like ours that incorporate genetic variation in functional traits and their response to climate gradients will lead to a better understanding of plant distributions as well as identifying populations anticipated to be maladapted to future environments.

     
    more » « less