Armbruster, W. S.

English

Portsmouth University Research Portal (Pure)

Multiple Origins of Serpentine-Soil Endemism Explained by Pre-existing Tolerance of 
Open Habitats 
 
 
W. Scott Armbruster1 
School of Biological Sciences, University of Portsmouth, Portsmouth PO1 2DY, UK  
Institute of Arctic Biology, University of Alaska, Fairbanks, AK 99775, USA 
Department of Biology, Norwegian University of Science and Technology, N-
7491Trondheim, Norway 
 
1email: scott.armbruster@port.ac.uk 
 
Plant specialization on soils derived from unusual parent materials is an important 
contributor to regional biodiversity. These stressful substrates include serpentine, gabbro, and 
other ultramafic rocks rich in heavy metals.  The effect of substrate on plant diversity is 
illustrated by serpentine soils in California: they comprise less than 1% of the surface of state 
(1), but serpentine endemics (species restricted to serpentine soils) make up about 10% of the 
flora (2).  How such “edaphic endemics” (plants restricted to stressful soils) evolve is a long-
standing question that remains largely unresolved.  For example, plant tolerance of serpentine 
soils may often involve trade-offs in competitive ability, and restriction to serpentine soil may 
reflect poor competitive ability on less stressful soils rather than obligate association (3,4,5), 
although possible counter examples exist (6).  A common feature of plant communities on 
stressful soils is the wide-spacing of plants and openness of the habitat.  Openness may itself 
be stressful for a variety of reasons (detailed below) (7,8,9).  In PNAS, Cacho & Strauss (10) 
use a novel comparative-experimental approach to assess explicitly the role of openness vs. 
soil chemistry as factors in the evolution of plant tolerance of, and endemism to, serpentine 
soils.   
Plants that tolerate and are endemic to stressful ultramafic (serpentine) soils have 
become a well developed system for the study of adaptation, speciation, endemism, 
competition, and community ecology (2,6,11).  Classic studies have shown the probable role 
of elemental imbalances (e.g.  high concentrations of heavy metals, including Ni, Co, Cu, Cr, 
Pb; low Ca:Mg ratios; low concentrations of macronutrients, etc.), although there is no 
consensus on the main causes of stress and species exclusion (2,6).  There may indeed be a 
diversity of causal factors, as might be expected from the diversity of plant lineages in which 
serpentine tolerance and endemism have evolved, each with different genetic and 
physiological starting points. Regardless of the physiological causes, there are well defined 
serpentine floras and vegetation types recognized in North America, including Cuba; Europe, 
including Britain; South Africa; and Oceania, among other regions.  The floras are 
characterized by very high endemism, and the vegetation is usually sparser and often more 
xeromorphic (appearing drought adapted) than nearby vegetation on “normal” soils (Figs. 
1A, B).      
The openness of the habitat may itself be a source of stress contributing to endemism.  
Several authors have found that the balance between competition (for light, water, and/or 
nutrients) and facilitation between neighboring plants in a landscape depends on the level of 
stress: in a benign landscape competition dominates, but in a stressful environment, 
facilitation dominates (8,9).  As the habitat gets more open, especially in hot, dry climates 
(e.g., summer in regions with Mediterranean climates), the paucity of neighbors means 
greater exposure to the drying effects of wind and high direct-radiation loads, as well as the 
stress of high leaf temperatures and potential UV damage.  Recent research has also shown 
that plants in sparsely vegetated sites are also more apparent to herbivores (e.g., more 
susceptible to attack by herbivorous insects), and such plants may have had to evolve 
expensive counter adaptations (e.g., increased chemical defenses and/or more cryptic foliage) 
(7).   
A series of studies from a remote corner of NE Alaska illustrates a possible biological 
connection between edaphic endemism and open habitats.  Studies in the region have noted 
the narrow distribution of possible relict plant species, disjunct from nearest relatives by 
hundreds of kilometers (e.g., 12,13,14).  Some of these endemics appeared, at first, to be 
restricted to greenstone (an ultramafic mineral) outcrops (12).  Later observations (13,14) and 
experiments (14) showed that all putative greenstone endemics were found also on a variety 
of other parent materials.  The taxa are indeed rare and disjunct, but endemic to south-facing 
slopes so steep and dry that they are largely open habitats with sparse vegetation. Thus plants 
adapted to the stress of dry, open habitats can have similar ecological behavior as edaphic 
endemics. This could lead one to ask if adaptation to open habitats might sometimes be the 
first step towards tolerance of ultramafic soils. 
Cacho & Strauss (10) address this and related questions by looking at the evolution of 
tolerance to elements associated with serpentine soils, and to open habitats in relation to soil 
shifts across the phylogeny of a group of wild mustards (Streptanthus and relatives; 
“streptanthoid mustards”) in which serpentine endemism has evolved 4-5 times (15). They 
use a powerful, but rarely realized approach in evolutionary-ecological research, that of 
integrating comprehensive sets of measurements and/or experiments into a molecular 
phylogeny (see 16) to gain insights into the evolutionary history of soil specialization.   
Intriguingly, Cacho and Strauss (10) find evidence that tolerance to open habitats 
appears to have evolved before tolerance of serpentine soils (Fig. 1C) and hence been a 
preaptation (pre-adaptation).  Cecchi et al . (17) also concluded recently that preaptations 
(e.g., for drought tolerance) have been critical in the origins of serpentine tolerance, but had 
no direct evidence to support their hypothesis.  Cacho and Strauss (10) also provide evidence 
that tolerance of stressful soil elements evolved in streptanthoid mustards coincident with, or 
after, switches to serpentine soils, rather than prior to switches to serpentine, as expected.  In 
addition, in a novel, common-environment, competition experiment, the authors show that 
plants from more open habitats have lower competitive abilities.  Importantly, this 
relationship is similar whether the plants are from bare habitats in serpentine-soil landscapes 
or from bare habitats in “normal”-soil landscapes.   
The multiple origins of serpentine tolerance in the streptanthoid mustards raise a long-
standing question in evolutionary biology: How do new ecological adaptations originate and 
why do parallelisms occur?  The answer in both cases may be that critical pre-existing 
features that enable an ecological shift are already in place.  A recent study by Christin et al. 
(18) found evidence for multiple parallel origins of C4-photosynthesis in grasses and that 
these shifts were contingent on appropriate pre-existing leaf anatomy (exaptation).  The 
parallels to the present study (10) are striking, Thus there seems to growing support for the 
idea that major adaptive transitions in evolution often, or even usually, occur through the 
prior establishment by chance of one or more preaptations (19; e.g., 20,21).  Once these 
preaptations are in place, it becomes much more likely that multiple independent parallel 
shifts (parallelisms) will occur, hence explaining the commonness of parallel evolution as is 
often observed in adaptive traits (e.g., 15,18,21).  Additional detailed phylogenetic-
comparative studies, such as this one (10), may show evolution by exaptation (preaptations 
acquiring new functions) to be the dominant theme wherever parallelisms are observed in 
groups of related species.  
___________________________________________________________________________ 
1. Kruckeberg AR (1984) California serpentines: flora, vegetation, geology, soils, and 
management problems (University of California Press, Berkeley). 
2. Brady KU, Kruckeberg AR, Bradshaw Jr HD (2005) Evolutionary ecology of plant 
adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266. 
3. Kruckeberg AR (1954) The ecology of serpentine soils III. Plant species in relation to 
serpentine soils. J Ecol 35:267–274. 
4. Grime JP (1977) Evidence for the existence of three primary strategies in plants and its 
relevance to ecological and evolutionary theory. Am Nat 111:1169–1194. 
5. Anacker BL (2014) The nature of serpentine endemism. Amer J Bot 101(2):219–224  
6. Powell KI, Knight TM (2009) Effects of nutrient addition and competition on biomass of 
five Cirsium species (Asteraceae), including a serpentine endemic. Int J Plant Sci 
170(7):918–925. 
7. Strauss SY, Cacho NI (2013). Nowhere to run, nowhere to hide: The importance of 
enemies and apparency in adaptation to harsh soil environments. Amer Naturalist 182:E1-
E14. 
8. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 
9:191–3.  
9. Oviedo R, et al. (2014) Facilitation allows plant coexistence in Cuban serpentine soils. 
Plant Biology 16(4):711-716.  
10. Cacho NI, Strauss SY (2014) Occupation of bare habitats, an evolutionary precursor 
to soil specialization in plants.  Proc Natl Acad Sci USA XX,ZZZ.  
11. Harrison S, Rajakaruna N (2011) Serpentine: The evolution and ecology of a model 
system (University of California Press, Berkeley, California, USA).  
12. Shacklette HT (1966) Phytoecology of a greenstone habitat at Eagle, Alaska. US 
Geological Survey Bulletin 1198-F.  
13. Batten AR, Murray DF, Dawe JC (1979) Threatened and endangered plants in selected 
areas of the BLM Fortymile Planning Unit Alaska. BLM Tech Rep BLM/AK/TR3:1–134. 
14. Wesser SD, Armbruster WS (1991) Species distribution controls across a forest-steppe 
transition: A causal model and experimental test. Ecol Monogr 61:323–342. 
15. Cacho NI, Burrell AM, Pepper AE, Strauss SY (2014) Novel nuclear markers inform the 
systematics and the evolution of serpentine use in Streptanthus and allies Thelypodieae, 
Brassicaceae). Mol Phylogenet Evol 72:71–81. 
16. Weber MG, Agrawal AA (2012) Phylogeny, ecology, and the coupling of comparative 
and experimental approaches. Trends Ecol Evol 27:394–403. 
17. Cecchi L, Coppi A, Selvi F (2011) Evolutionary dynamics of serpentine adaptation in 
Onosma (Boraginaceae) as revealed by ITS sequence data. Plant Systematics Evolution 
297:185-199 
18. Christin PA, et al. (2013) Anatomical enablers and the evolution of C-4 photosynthesis in 
grasses. Proc Natl Acad Sci USA 110:1381-86.   
19. Gould SJ, Vrba ES. (1982) Exaptation - a missing term in the science of form. 
Paleobiology 8(1):4-15.  
20. Pellmyr O (1997) Pollinating seed eaters: Why is active pollination so rare? Ecology 
78:1655-1660.  
21. Armbruster WS, Lee J, Baldwin BG (2009) Macroevolutionary patterns of defense and 
pollination in Dalechampia vines: adaptation, exaptation, and evolutionary novelty. Proc 
Natl Acad Sci USA 106:18085–90. 
 
 
 
 
 
 
Figure 1.  Evolution of serpentine-soil endemism from occupation of “normal” soils is 
apparently contingent on prior adaptations to occurring in open habitats.  A. Dense 
vegetation characteristic of “normal” soils in Napa County, California.  Pink flowers 
are Collinsia sparsiflora Fisch. & C.A. Mey, a species with “normal” and serpentine 
ecotypes.  Photo credit: WS Armbruster.  B. Open, sparse vegetation on a serpentine 
outcrop in nearby Lake County, California.  Pink flowers in foreground are Clarkia 
gracilis subsp. tracyi (Jeps.) Abdel-Hameed & R. Snow, a subspecies largely 
restricted to serpentine soils. Photo credit: WS Armbruster.   C. Maximum-credibility 
tree of the streptanthoid mustards, showing inferred evolution of open-habitat 
adaptations (maximum-likelihood ancestor-state reconstruction; shading on branches, 
with darker indicating occurrence in more open habitats; modified with permission 
from Fig. S4 in (10-Cacho & Strauss 2014).  Arrows indicate inferred origins of 
serpentine endemism (> 87% of records from serpentine soils; red) and serpentine 
tolerance (>11%, <87% of records from serpentine soils; violet), evolving from 
occupation of “normal” soils (branches to left of the violet or red arrows; data from 
(10-Cacho & Strauss 2014)). Soil-type optimization on branches used ordered 
parsimony, where serpentine tolerance is assumed to be a precursor of serpentine 
endemism.   (To simplify the diagram, inferred coincident origins of tolerance and 
endemism are not shown.)  
 
 
 
 
 
 
 
 
 


Multiple origins of serpentine-soil endemism explained by preexisting tolerance of open habitats

Name not available

http://eprints.port.ac.uk/id/document/42165

Multiple origins of serpentine-soil endemism explained by preexisting tolerance of open habitats

Abstract

Similar works

Full text

Available Versions

Portsmouth University Research Portal (Pure)

Name not available