Annals of Botany 104: vii –x, 2009
Available online at www.aob.oxfordjournals.org
Book Review
doi:10.1093/aob/mcp194
Published electronically: 18 August 2009
Biology and evolution of ferns
and lycophytes
Ranker TA, Haufler CH. eds.
2008.
Cambridge, UK: Cambridge
University Press. £35
( paperback). 480 pp.
About once every decade for the
last 80 years, a volume has been
produced that reports comprehensively on recent developments
in pteridology. Some have an
emphasis on particular aspects,
such as phylogeny, cytogenetics or gametophytes, while
others have a broader coverage. Together with several substantial proceedings of conferences, these books have helped to
maintain the momentum of interest in ferns and lycophytes.
With the current changes in fashion in botanical curricula
and the reduction in research support for pteridology, the
stimulus of another major publication of this kind was
needed. Ranker and Haufler have followed in the tradition
of Verdoorn’s multi-authored compendium Manual of
Pteridology (1938) and assembled contributions that include
a broad selection of topics across the range currently being
investigated. They cover all the plant groups traditionally
included in the ‘Pteridophytes’, but avoid the use of the
name in the title in recognition of the current view that the
groups do not share a common ancestor and therefore a collective noun is no longer valid (this has robbed us also of the term
‘pteridologist’, for which there is no convenient alternative.)
The 16 chapters are grouped into four parts: ‘Development
and Morphogenesis’ (103 pages), ‘Genetics and Reproduction’
(94 pages), ‘Ecology’ (102 pages) and ‘Systematics and Evolutionary Biology’ (167 pages). The list of 28 authors includes
several of the elder statesmen of today’s ‘pteridology’, along
with some of the rising stars. Twenty authors are based in the
USA, the remainder with addresses in Canada, Mexico,
Japan, Sweden, Switzerland and the UK. This may reflect the
fact that both editors are from the USA as much as it mirrors
the geographical distribution of current pteridological activity,
but it is true that in the UK at least there are now few active
research pteridologists who can contribute to such a volume.
The intended readership is stated to be advanced undergraduates, graduates and academic researchers. This means that each
chapter should provide sufficient background for those new to
the field, a survey of recent developments to bring the reader
up to date, and a synthesis of ideas to stimulate further investigation. This in turn means that those who have read earlier
accounts might be disappointed to find that some of the
content is familiar, particularly in the areas where research progress is slow. However, this is balanced by the fact that this
volume provides a one-stop source for beginners.
In Chapter 1, M. Wada discusses ‘Photoresponses in fern
gametophytes’. He describes the investigation of most of the
growth responses and intracellular reactions (from chloroplast
movement to nuclear division) to monochromatic or polarized
light, and the current understanding of the photoreceptors
(more than 10 already identified in Adiantum) and the mechanisms involved. This account would of course be useful to students new to the topic, but should also be read by fern
ecologists interested in the gametophyte in the natural environment and by plant physiologists researching photoresponses in
angiosperms.
In Chapter 2, ‘Alternation of generations’, E. Sheffield presents a brief review of the familiar and fundamental issue of
the alternation of gametophyte and sporophyte generations.
This is nowhere more conspicuous than in the ferns and lycophytes, the only organisms in which both phases are capable of
independent, free-living existence. There is little that is new to
report about the origin and adaptive success of this two-phase
life cycle, but the availability of new techniques promises progress in our understanding of the controlling mechanisms. A
review of the events and modifications of the homosporous
life cycle is illustrated by some excellent SEM photographs;
heterosporous life cycles are not considered. The brevity of
the treatment of obligate apomixis, despite its adaptive importance, is perhaps an indication that there have been few recent
investigations of its mechanism or ecological success.
In Chapter 3, ‘Meristem organisation and organ diversity’,
R. Imaichi presents a concise, clear and well-ordered review
of apical development of stems and stem branches, leaves
and roots. Also covered are the specialized rhizomes of the
whisk ferns, the rhizophores unique to the Selaginellaceae,
and the rhizomorphs found only in the Isoetaceae. Progress
is slow in this field (only 10 of the 91 papers quoted were
written in the last 10 years) and Imaichi covers the major
developments of the last 40 years. Most pteridologists, whatever their specialism, would find this account interesting
because the events at the meristems, and particularly the
apical meristems, determine the conspicuous characteristics
that define the ferns, lycophytes and their component groups.
Chapter 4, ‘Population genetics’ by T. Ranker and
J. M. O. Geiger, provides a useful critical review of 40 years
of investigation by a variety of techniques into population genetics and the reproductive biology fundamental to it. Most
observations relate to homosporous ferns and increasingly in
recent years depend on molecular techniques. On the basis
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Book Review
of the small proportion of the world flora that has been studied,
a coherent picture is emerging. Most diploid fern species form
mainly unisexual gametophytes and are to a greater or lesser
extent outcrossing, with levels of genetic diversity no lower
than seed plants. However, some pioneer species that colonize
new habitats, many polyploid species, and those with subterranean gametophytes are able to inbreed by intra-gametophytic
selfing of bisexual gametophytes. Further clarification will
require the use of a broader range of species and the wider
application of molecular techniques.
J. J. Schneller, who has been a source of interesting observations on fern reproductive biology for 30 years, has contributed Chapter 5, ‘Antheridiogens’. This provides a useful
summary of the history of investigations, mostly in the laboratory, into sex determination by antheridiogen pheromones in
gametophytes of homosporous ferns. The account highlights
the need for more research, especially into the role of antheridiogens in nature, the occurrence of antheridiogens in other
(especially tropical) species, the interaction of antheridiogens
with the phytochrome system, and the molecular aspects of
genetic regulation of sex determination.
In Chapter 6, ‘Structure and evolution of fern plastid
genomes’, P. G. Wolf and J. M. Roper describe the progress
in mapping the chloroplast genome. It is nearly 20 years
since restriction mapping revealed that lycophytes lack an
inverted repeat (IR) present in all other extant vascular
plants. This approach has been succeeded by complete
genome mapping (first achieved for Adiantum capillus-veneris
in 2003 by Wolf et al.) and PCR mapping of the gene order of
the IR sequence. Recent results have shown that the rare
changes in the structure of the evolutionarily conservative IR
provide phylogenetic data. Wolf and Roper describe the methodological approach and present previously unpublished
results. New molecular techniques promise significant developments in the near future. The implications of the results
will interest all pteridologists, even if the methods can be
fully appreciated only by other molecular phylogeneticists.
In a parallel chapter (Chapter 7), T. Nakazato, M. S. Barker,
L. H. Rieseberg and G. J. Gastony consider the ‘Evolution of
the nuclear genome of ferns and lycophytes’. Genomic studies
in these seedless plants lag behind those in flowering plants;
the first linkage map of a fern was not published until 2006,
more than 20 years after the first for angiosperms. The
results from new molecular technologies, including linkage
mapping and targeted gene silencing, are fine-tuning the longestablished theory that homosporous fern and lycophyte
genomes with large numbers of chromosomes are the consequence of repeated genome doubling events followed by
gene silencing or even gene elimination. Full resolution of
the issues relating to the unique features of genome evolution
in ferns and lycophytes requires further research into various
aspects, from meiotic pairing, C values, gene expression and
gene mapping to whole-genome sequencing. Much of the
recent work has focussed on Ceratopteris richardii, a model
fern with a conveniently short life cycle; in future it will be
necessary to widen the range of plants analysed to include
the heterosporous ferns and lycophytes as well as other homosporous species, both palaeopolyploids and neopolyploids,
representative of all the main phylogenetic lineages.
viii
Little has been written about tropical fern ecology over the
last 100 years but in Chapter 8, ‘Phenology and habitat specificity of tropical ferns’, K. Mehltreter, one of those who has
helped to stimulate interest in the last few years, has reviewed
recent investigations of habitat preferences and periodicity in
biological processes. The facts presented in this chapter
reveal not how much but how little we know about tropical
fern ecology. There is a need for more quantitative field data
obtained over long periods and across a wide range of
species and habitats, and in conjunction with the investigations
of physiology, biochemistry, morphology and genetics,
without which fern ecology is unlikely to be fully understood.
This draws our attention to the fact that there is no chapter in
this book on the physiology and biochemistry of ferns, reflecting the current lack of interest. The absence of any mention of
the gametophytes’ role in determining phenology or habitat
specificity is no doubt in deference to the chapter that follows.
Chapter 9, ‘Gametophyte Ecology’ by D. R. Farrar,
C. Dassler, J. E. Watkins, Jr. and C. Skelton, is one of the
longest chapters in the book and goes some way towards reversing the past neglect in print of the gametophyte in natural
habitats. No one is better qualified than Farrar to review this
topic, although in one or two places this chapter appears to
have been written in separate sections by different authors
and then ‘bolted’ together. With a focus on leptosporangiate
species, the account summarizes what little has been published
and adds some new unpublished observations. Contrary to
popular belief, the familiar short-lived cordiform prothallus
is not the archetypical fern gametophyte; it is an evolutionarily
advanced form that is adapted to disturbed terrestrial microhabitats and is largely restricted to modern leptosporangiate
species. Most older fern groups, and those species of the
more recent Polypodiales that occupy the more stable epiphytic habitats, together present a diverse array of long-lived,
elongate and proliferating gametophytes, some with vegetative
propagules. The chapter finishes with some interesting original
observations on differences between laboratory-raised and
field-grown gametophytes, which in turn point towards some
of the factors influencing development in the wild. Because
of the central role of the gametophyte generation in establishment and reproduction, this chapter should be essential reading
for everyone with an interest in fern ecology.
Chapter 10, ‘Conservation biology’ by N. N. Arcand and
T. A. Ranker, presents a concise outline of the issues relating
to the conservation of ferns and lycophytes, in particular
endemic species of high conservation priority and species in
identified diversity ‘hot-spots’. It covers the case for conservation, the range of threats to diversity and their causes, and the
different practical approaches to in situ and ex situ conservation. Although habitat restoration is highlighted, there is no
discussion of the contentious issues relating to re-introduction
( planting at sites where a species once grew but has become
extinct) and augmentation ( planting in populations endangered
because of their very small number of individuals) using
ex situ-raised plants. The need for more evaluation of conservation requirements, and for more research into fern and lycophyte ecology and in situ development, is made clear. The
comprehensive list of relevant literature, mostly from the last
10 years, will be useful.
Book Review
In Chapter 11, ‘Ex situ conservation of ferns and
lycophytes – approaches and techniques’, V. C. Pence
enlarges on one aspect of practical conservation, touched
upon in the previous chapter and likely to be of growing interest as the various available techniques are developed. In most
cases, the various types of ex situ gene banks are derived from
initial samples taken as spores from surviving wild plants or
natural soil spore banks, but where spores are not available
or not viable, techniques known as ‘in vitro collecting’
(IVC) are being developed for establishing tissue cultures
from excised explants obtained from plants in the wild
without harming them. It is unlikely that there is one method
of ex situ conservation that is optimal for all species, so
more research into the effectiveness of alternative techniques
and the requirements of individual species, as well as the
physiology of spores and plant tissues in storage, is needed
in order to facilitate the establishment of more long-term conservation germplasm banks.
Chapter 12, ‘Species and speciation’ by C. H. Haufler, will
be largely familiar to anyone who has read earlier reviews by
this author, but it is convenient to have this well-written
account along with all the other topics. There was a time
when speciation in ferns and lycophytes was considered to
be a less dynamic process than in angiosperms, but this is
not so. Primary speciation (diploid divergence after geographic
or ecological isolation despite the capacity for wide spore dispersal), secondary speciation (involving genetically isolated
autopolyploids, ecological isolation in rare fertile hybrids,
and allopolyploids derived from sterile hybrids), and tertiary
speciation (divergence in polyploids, sometimes involving
gene silencing and ‘diploidization’) have all been detected in
one or other group of ferns and lycophytes. Haufler issues a
plea for more research into the role of the gametophyte in
defining habitat specificity because ecological specialization
in peripheral populations can be an important step in speciation, particularly in tropical species. We must now view
ferns not as a relatively few widely dispersed species but as
many, more narrowly defined, often cryptic species.
In Chapter 13, ‘Phylogeny and evolution of ferns;
a paleontological perspective’, G. R. Rothwell and
R. A. Stockey consider the early stages of that phylogeny.
They state that their account is intended for the nonpaleontologist, but the reader will benefit considerably from
being familiar with the morphological and phylogenetic terminology as well as the (American) names of the geological
periods and their dates. The authors’ interpretation of the
relationships among euphyllophytes (i.e. excluding lycophytes) is not the only one and the concentrated text is not
an easy read, but it is a good reference source. Throughout,
only the sporophyte is considered, implying that no gametophytes have been found in the fossil record. The chapter is
illustrated by more than 70 photographs but much of their
potential value is lost because they are so small, with up to
20, together with captions, on a single page. The authors
finish with a plea for including fossil evidence in any phylogenetic analysis; basing it entirely on studies of living representatives often leads to a different interpretation.
After more than 170 years of publication on the subject, the
literature on biogeography of ferns and lycophytes is now
overwhelming, so in Chapter 14, ‘Diversity, biogeography
and floristics’, R. Moran has limited himself to three
interrelated topics: diversity, long-distance dispersal, and
vicariance, and to 214 references. Diversity increases from
the temperate latitudes to the equator and is greatest in the
middle altitudes of mountains. The whole of Britain and
Ireland has just over 70 native species whereas a single tree
in Costa Rica can contain 50 species. While mountains can
form barriers to migration of species, there is considerable circumstantial evidence for long-distance dispersal. Molecular
phylogeny also indicates a role for continental drift and
climate change in explaining some instances of disjunct distribution. Moran finishes by highlighting the need for more plant
collecting and publication of floras and more research into, for
example, speciation rates and the influence of ploidy, morphology and life cycle characteristics on ecological and geographical distribution. Progress will be accelerated by greater
dissemination of information via the web and by the questions
raised by new phylogenetic trees derived from improved DNA
sequencing.
In Chapter 15, ‘Fern phylogeny’, E. Scheuttpelz and
K. M. Pryer present a series of diagrams of the fern ‘tree of
life’ with accompanying commentary and supporting references. This clearly summarizes the current hypotheses concerning fern relationships based on molecular phylogenetic
analysis in a way that those not routinely immersed in the intricacies can easily refer to and follow. The account starts with
the early vascular plant divergences that explain the abandonment of the concept of ‘pteridophytes’ (a term previously used
to include all the spore-bearing and ‘seed-free’ plants) and that
justify the inclusion of horsetails and whisk ferns within a
broadly defined group of ‘ferns’. It then progresses through
the early separation of leptosporangiates from other ferns
and the divergence of the monophyletic older families like
Osmundaceae and Hymenophyllaceae from the remainder, to
the relationships between the leptosporangiate families,
including the ‘tree ferns’ (not all have trunks), heterosporous
water ferns, and the ‘Polypods’, a group united by having sporangia with a vertical annulus interrupted by the stalk, and
which contains the majority of fern species. Within these
groupings, relationships between genera and selected species
are suggested. At this level there are many uncertainties, as
well as inconsistencies between conclusions based on molecular analyses and those based on morphology. However, this
framework derived from DNA sequence analysis provides a
focus for further resolution of evolutionary patterns.
The final Chapter 16, ‘Fern classification’, is essentially an
update of the 2006 paper (in Taxon) by the same authors:
A. R. Smith, K. M. Pryer, E. Schuettpelz, P. Korall,
H. Schneider and P. Wolf. The classification is based on the
consensus relationships that are presented in Chapter 15 by
two of these authors; the common authorship results in close
compatability, but also a little repetition, between the two
chapters. Ferns are described as a monophyletic group
of about 9000 species (compare with the estimate of over
12 000 given in Chapter 14) with several shared characteristics.
Accounts are presented of 37 fern families in 11 orders within
four classes: Psilotopsida, Equisetopsida, Marattiopsida and
Polypodiopsida. For each family there is a description of characters, the numbers and names of genera, chromosome
numbers, synonyms, references and outstanding classification
ix
Book Review
problems. Although recent molecular analyses have produced
some surprises, and despite the need to resolve some circumscriptions, many of the families and monotypic genera that had
been recognized in past major classifications, mostly morphologically based, still have strong support, with evidence of
monophyly. The chapter finishes with appendices listing
familial and generic names, both those accepted by the
authors and others. The family summaries and genus placements, although no doubt already familiar to those who
work in the field of fern classification, provide a useful reference source for those who do not.
Throughout the volume, which finishes with a comprehensive index, the editors’ beneficial influence is apparent in the
consistent approach of many of the chapters (introduction
and plan, historical survey, review of important recent
advances, future directions, and a comprehensive list of relevant references, more than 200 in some chapters) and in the
commendable rarity of typographical errors. I found only
three that were potentially misleading. First, on page 368,
line 2, ‘13 600’ should be ‘1 360’; second, ‘Smith et al,
2006a’ in Table 16.1, page 418, should be ‘Smith et al,
2006b’; third, the editors will not be happy that ‘homoeologous’ was changed to ‘homologous’ in several places on
pages 112, 178, and 179 after they handed over the final draft.
This book will be indispensable for complementing any fern
biology or systematics courses still taught at university. It will
provide essential background information for those beginning
research in any of the areas covered. Botanists working in
similar areas of seed-plant biology will benefit from reading
about the parallel processes in a different vascular plant
group. However, for all but the most dedicated of amateur
fern enthusiasts, many chapters will probably appear to be
too detailed and technical, despite the fact that contained
within them are statements that might well interest them.
Adrian Dyer
E-mail [email protected]
L I T E R AT U R E CI T E D
Smith AR, Pryer KM, Schuettpelz E, Korall P, Schneider H, Wolf PG.
2006. A classification for extant ferns. Taxon 55: 705– 731.
Verdoorn F. (ed). 1938. Manual of pteridology. The Hague: Martinus Nijhoff.
Wolf PG, Rowe CA, Sinclair RB, Hasebe M. 2003. Complete nucleotide
sequence of the chloroplast genome from a leptosporangiate fern,
Adiantum capillus-veneris L. DNA Research 10: 59–65.
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