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Hardly a Relict: Freezing and the Evolution of Vesselless Wood in Winteraceae

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Feild, TS and Brodribb, TJ and Holbrook, NM (2002) Hardly a Relict: Freezing and the Evolution of Vesselless Wood in Winteraceae. Evolution, 56 (3). pp. 464-478. ISSN 0014-3820

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Abstract

The Winteraceae are traditionally regarded as the least-specialized descendents of the first flowering plants,
based largely on their lack of xylem vessels. Since vessels have been viewed as a key innovation for angiosperm
diversification, Winteraceae have been portrayed as declining relicts, limited to wet forest habitats where their tracheidbased
wood does not impose a significant hydraulic constraints. In contrast, phylogenetic analyses place Winteraceae
among angiosperm clades with vessels, indicating that their vesselless wood is derived rather than primitive, whereas
extension of the Winteraceae fossil record into the Early Cretaceous suggests a more complex ecological history than
has been deduced from their current distribution. However, the selective regime and ecological events underlying the
possible loss of vessels in Winteraceae have remained enigmatic. Here we examine the hypothesis that vessels were
lost as an adaptation to freezing-prone environments in Winteraceae by measuring the responses of xylem water
transport to freezing for a diverse group of Winteraceae taxa as compared to Canella winterana (Canellaceae, a close
relative with vessels) and sympatric conifer taxa. We found that mean percent loss of xylem water transport capacity
following freeze-thaw varied from 0% to 6% for Winteraceae species from freezing-prone temperate climates and
approximately 20% in those taxa from tropical (nonfreezing) climates. Similarly, conifers exhibit almost no decrease
in xylem hydraulic conductivity following freezing. In contrast, water transport in Canella stems is nearly 85% blocked
after freeze-thaw. Although vessel-bearing wood of Canella possesses considerably greaterhydraulic capacity than
Winteraceae, nearly 20% of xylem hydraulic conductance remains, a value that is comparable to the hydraulic capacity
of vesselless Winteraceae xylem, if the proportion of hydraulic flow through vessels (modeled as ideal capillaries) is
removed. Thus, the evolutionary removal of vessels may not necessarily require a deleterious shift to an ineffective
vascular system. By integrating Winteraceae’s phylogenetic relationships and fossil history with physiological and
ecological observations, we suggest that, as ancestors of modern Winteraceae passed through temperate conditions
present in Southern Gondwana during the Early Cretaceous, they were exposed to selective pressures against vesselpossession
and returned to a vascular system relying on tracheids. These results suggest that the vesselless condition
is advantageous in freezing-prone areas, which is supported by the strong bias in the ecological abundance of Winteraceae
to wet temperate and tropical alpine habitats, rather than a retained feature from the first vesselless angiosperms.
We believe that vesselless wood plays an important role in the ecological abundance of Winteraceae in Southern
Hemisphere temperate environments by enabling the retention of leaves and photosynthesis in the face of frequent
freeze-thaw events.

Item Type: Article
Keywords: Angiosperm evolution, Canellaceae, Drimys, freezing stress, Winteraceae, xylem evolution.
Journal or Publication Title: Evolution
Page Range: pp. 464-478
ISSN: 0014-3820
Identification Number - DOI: 10.1111/j.0014-3820.2002.tb01359.x
Additional Information:

"The definitive version is available at www.blackwell-synergy.com"

Date Deposited: 03 Dec 2007 02:03
Last Modified: 18 Nov 2014 03:25
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