Download Taxonomy and Evolution of the Cotton Genus, Gossypium

Published April 23, 2015
Taxonomy and Evolution
of the Cotton Genus, Gossypium
Jonathan F. Wendel* and Corrinne E. Grover
Abstract
We present an overview of the taxonomy of Gossypium L. (the cotton genus) and its
evolutionary history. Gossypium contains more than 50 recognized species, including
several recently described, distributed in arid to semiarid regions of the tropics and
subtropics. Diversity in Gossypium has been promoted by two seemingly unlikely processes: transoceanic, long-distance dispersal and wide hybridization among lineages
that presently are widely separated geographically. Included are four species that were
independently domesticated for their seed fiber—two diploids from Africa–Asia and
two allopolyploids from the Americas. This repeated domestication of different wild
progenitors represents a remarkable case of human-driven parallel evolution. Morphological variation in Gossypium is extensive; growth forms in the genus range from
sprawling herbaceous perennials to ?15-m-tall trees, representing a notable array of
reproductive and vegetative characteristics. Equally impressive is the striking cytogenetic and genomic diversity that emerged as Gossypium diversified and spread
worldwide, ultimately spawning eight groups of closely related diploid (n = 13) species
(i.e., genome groups A through G, and K). DNA sequence data place the origin of Gossypium at about 5 to 10 million years ago (mya), which rapidly diversified into these major
genome groups shortly thereafter. Allopolyploid cottons appeared within the last 1 to 2
million years, a consequence of the improbable transoceanic dispersal of an A genome
taxon to the New World and subsequent hybridization with an indigenous D genome
diploid. Diversification of the nascent allopolyploid gave rise to three modern lineages
containing seven species, including the agronomically important G. hirsutum L. and G.
barbadense L.
B
ecause of its economic importance, the cotton genus (Gossypium L.) has been
of interest to agricultural scientists, taxonomists, and many other kinds of
biologists. Accordingly, a considerable amount is understood regarding the origin and diversification of the genus, its basic plant biology, and its properties as
a crop plant (Paterson, 2009; Stewart et al., 2010; Wendel et al., 2009, 2010, 2012).
Increasingly over the past two decades, classic taxonomic questions such as the
origin of the polyploid species, the relationships among species and species
Abbreviations: mya, million years ago.
Jonathan F. Wendel and Corrinne E. Grover ([email protected]), Dep. of Ecology,
Evolution, and Organismal Biology, Bessey Hall, Iowa State University, Ames, IA 50011.
*Corresponding author ([email protected]).
doi:10.2134/agronmonogr57.2013.0020
Copyright © 2015. ASA, CSSA, and SSSA, 5585 Guilford Road, Madison, WI 53711, USA.
Cotton. 2nd. ed. David D. Fang and Richard G. Percy, editors. Agronomy Monograph 57.
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groups, and the origins of the domesticated forms from their wild progenitors
have been revisited using modern molecular technologies (Wendel et al., 2009,
2010, 2012; Wendel and Cronn, 2003). One of the salient features of the genus
is that its history is so encompassing in scope, involving a global phylogenetic
diversification and a repeated history of transoceanic dispersal. A remarkable
consequence of this global spread and natural diversification has been that it provided the opportunity for different ancient human cultures on several continents
to independently domesticate four different cotton species—two allopolyploids
from the Americas, G. hirsutum and G. barbadense, and two diploids from Africa–
Asia, G. arboreum L. and G. herbaceum L. The canvas for this human history is
the natural evolutionary diversification of the genus, one that involves multiple,
seemingly impossible hybridization events, often between lineages that presently
are geographically disjunct or even on different continents, as well as multiple,
remarkable cases of transoceanic, long-distance dispersals. These twin themes of
cryptic intergenomic introgression or hybridization and long-distance dispersal
have repeatedly come into play as the genus diversified and colonized much of
the arid to semiarid regions of the tropics and subtropics.
A wealth of recent studies have provided new insights into Gossypium taxonomy and diversity, suggesting that it is an appropriate time to update our
understanding of the evolution, taxonomy, and biogeographic history of the
genus. Here we provide such an update, drawing on our earlier reviews (Wendel
et al., 2009, 2010, 2012; Wendel and Cronn, 2003) and with new syntheses.
Emergence of the Genus Gossypium
The cotton genus belongs to the Gossypieae, a small taxonomic tribe that includes
only nine genera, eight of which are classically recognized (Fryxell, 1968, 1979)
and one that is a new segregate from Cienfuegosia (Phuphathanaphong, 2006). Five
of these genera are small with restricted geographic distributions (Fryxell, 1968,
1979; Phuphathanaphong, 2006) including Lebronnecia (Marquesas Islands), Cephalohibiscus (New Guinea, Solomon Islands), Gossypioides (East Africa, Madagascar),
Thepparatia (known only from the type locality in Northern Thailand) and Kokia
(Hawaii). The tribe also includes four moderately sized genera with broader geographic ranges: Hampea (21 neotropical species), the relatively diverse Cienfuegosia
(25 species from the neotropics and parts of Africa), Thespesia (17 tropical species),
and Gossypium, whose 50+ species (Fryxell, 1992) make it the largest and most
widely distributed genus in the tribe. Thus, in aggregate this small taxonomic
tribe has achieved an expansive geographic range, though many of the included
taxa are quite rare and/or narrowly distributed.
Molecular phylogenetic analyses have shed light on three important aspects
of the evolutionary history of the tribe (Cronn et al., 2002; Seelanan et al., 1997).
First and foremost is that despite their extensive distribution and extraordinary
diversity, the group of species that belong to Gossypium do constitute a single
natural lineage. A second important revelation has been the identity of the closest relatives of Gossypium, that is, the African–Madagascan genus Gossypioides
and the Hawaiian endemic genus Kokia. This is unsuspected finding, given their
biogeography and lower chromosome number (n = 12), yet it is quite important
in that they may serve as outgroups in phylogenetic analyses, which provides an
essential context both for studying evolutionary patterns and processes within
Taxonomy and Evolution of the Cotton Genus, Gossypium
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Gossypium and for understanding genome evolution. The third important insight
gained from these molecular analyses was the provision of a temporal component to the major divergences. Using sequence divergence data as a proxy for
time (i.e., a “molecular clock”), Seelanan et al. (1997) suggested that Gossypium
diverged from Kokia and Gossypioides circa 12.5 mya, an estimate bolstered by a
later, more extensive data set containing 10 different nuclear genes (Cronn et al.,
2002). Collectively, all molecular data suggest that Gossypium diverged from its
closest relatives approximately 10 to 15 mya during the Miocene and acquired its
modern, worldwide distribution by multiple transoceanic dispersals combined
with regional speciation.
Diversification of the Diploid Cotton Species
From the time of origin 5 to 10 mya, Gossypium experienced rapid speciation and
diversification, while also achieving a nearly worldwide distribution containing
several primary centers of diversity in the arid or seasonally arid tropics and subtropics (Table 1). Species-rich regions include Australia, especially the Kimberley
region in NW Australia; the Horn of Africa and southern Arabian Peninsula; and
the western part of central and southern Mexico. The taxonomy of the genus has
been well studied (Cronn et al., 2002; Fryxell, 1979, 1992; Hutchinson et al., 1947;
Saunders, 1961; Seelanan et al., 1997; Watt, 1907), with the taxonomic classification
of Fryxell (1979, 1992) being the most modern and widely followed. In this treatment, species are grouped into four subgenera and eight sections (Table 1). The
Table 1. Diversity and geographic distribution of the major lineages of Gossypium.
Genomic placements and taxonomic status of species enclosed by parentheses are
yet to be validated by cytogenetic and other means.
Genome
(no. of species) Recognized species
A (2)
G. arboreum, G. herbaceum
B (3–4)
G. anomalum, G. triphyllum, G. capitis-viridis, (G.
trifurcatum)
C (2)
G. sturtianum, G. robinsonii
D (13–14)
G. thurberi, G. armourianum, G. harknessii, G.
davidsonii, G. klotzschianum, G. aridum, G. raimondii,
G. gossypioides, G. lobatum, G. trilobum, G. laxum, G.
turneri, G. schwendimanii, (Gossypium sp. nov.)
E (5–9)
G. stocksii Mast., G. somalense (Gurke) J.B. Hutch., G.
areysianum Deflers, G. incanum (O. Schwartz) Hillc.,
G. trifurcatum, (G. benadirense), (G. bricchettii), (G.
vollesenii Fryxell), (G. trifurcatum)
F (1)
G. longicalyx
G (3)
G. bickii, G. australe, G. nelsonii
K (12)
G. anapoides, G. costulatum, G. cunninghamii, G.
enthyle Fryxell et al., G. exiguum Fryxell et al., G.
londonderriense Fryxell et al., G. marchantii, G. nobile
Fryxell et al., G. pilosum Fyxell, G. populifolium (Benth.)
F. Muell. ex Tod., G. pulchellum (C.A. Gardner) Fryxell,
G. rotundifolium Fryxell et al.
AD (7)
G. hirsutum, G. barbadense, G. tomentosum, G.
mustelinum, G. darwinii, G. ekmanianum, Gossypium
sp. nov.†
Geographic distribution
Africa, Asia
Africa, Cape Verde
Islands
Australia
primarily Mexico, with
range extensions
into Peru, Galapagos
Islands, Arizona
Arabian Peninsula,
Northeast Africa,
Southwest Asia
East Africa
Australia
Northwest Australia,
Cobourg Peninsula,
Northern Territory,
Australia
New World tropics
and subtropics,
including Hawaii, the
Wake Atoll, and the
Galapagos Islands
† J.F. Wendel, C.E. Grover, J. Jareczek, and J.P. Gallagher, unpublished data, 2014.
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classification represents the accumulated scientific understanding that emerged
both from basic plant exploration and taxonomic and evolutionary study. While
these species groupings are based primarily on morphological and geographical
evidence, most infrageneric alignments are congruent with subsequent cytogenetic and molecular data sets (Endrizzi et al., 1985; Wendel and Albert, 1992;
Wendel et al., 2009, 2010).
The current circumscription of Gossypium presently includes approximately
50 species (Fryxell, 1992), although new species continue to be discovered (Alvarez and Wendel, 2006; Grover et al., 2014; Krapovickas and Seijo, 2008; Stewart et
al., 2015; Ulloa et al., 2006). Morphologically, the genus is exceptionally diverse;
species morphologies range from fire-adapted, herbaceous perennials with massive underground rootstocks in NW Australia to trees in SW Mexico that escape
the dry season by dropping their leaves. Corolla colors span a rainbow of blue to
purple [G. triphyllum (Harv.) Hochr.], mauves and pinks (G. sturtianum J.H. Willis,
or “Sturt’s Desert Rose,” the official floral emblem of the Northern Territory, Australia), whites and pale yellows (NW Australia, Mexico, Africa–Arabia), and even
a deep sulfur-yellow (G. tomentosum Nutt. ex Seem., Hawaii). Seed coverings are
equally diverse; these range from nearly glabrous to the naked eye (e.g., G. klotzschianum Andersson and G. davidsonii Kellogg), to short, stiff, dense, brown hairs
that aid in wind dispersal (G. australe F. Muell and G. nelsonii Fryxell), to the long,
fine, white fibers that characterize highly improved forms of the four cultivated
species (Fig. 1). There are even seeds that produce fat bodies to facilitate ant-dispersal (Seelanan et al., 1999).
In addition to the remarkable morphological diversity, the genus also experienced extensive chromosomal evolution during diversification (Baudoin et al.,
2009; Endrizzi et al., 1985). Despite sharing the same chromosome number (n =
13), genome sizes among the diploid species vary more than threefold (Hendrix
and Stewart, 2005). Among closely related species, chromosome morphology is
quite similar, as is demonstrated by the ability of closely related species to form
hybrids that undergo normal meiotic pairing and that often experience high F1
fertility. In contrast, crosses between more distantly related species are often difficult to generate, with the few successful hybrids typically experiencing meiotic
abnormalities. Extensive observations concerning the pairing behavior, chromosome sizes, and relative fertility in interspecific hybrids ultimately led to the
clustering of closely related species into “genome groups,” designated by single-letter genome symbols (Beasley, 1941). Currently, there are eight recognized
diploid genome groups (A through G, plus K) (Endrizzi et al., 1985; Stewart, 1995),
whose species inclusions are largely congruent with taxonomic and phylogenetic
placements.
A temporal framework for the origin of Gossypium and its diversification is
provided by sequence divergence data serving as a proxy for time (Senchina et al.,
2003). These analyses indicate that Gossypium diverged from its closest relatives
during the Miocene approximately 10 to 15 mya to originate approximately 5 to
10 mya, and these estimates of divergence times have recently been supported by
an enormous amount of new sequence data derived from a global assembly of
expressed sequence tags (Flagel et al., 2012). A consideration of the near worldwide distribution of species combined with their phylogenetic history (Fig. 2),
relative to plate tectonic history, indicates that the evolution of Gossypium has
involved multiple episodes of transoceanic dispersal. Minimally, these include
Taxonomy and Evolution of the Cotton Genus, Gossypium
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Fig. 1. Representative seed and trichome diversity in Gossypium. Seed and trichome
size and morphology are exceedingly variable in the genus. Most wild species have
relatively small seeds (<5 mm in any dimension) with equally short fibers. Long
(spinnable) fiber evolved only once, in the ancestor of modern A genome cottons,
which subsequently donated this capacity to modern allopolyploid species, including
the commercially important G. hirsutum and G. barbadense, at the time of allopolyploid
formation. Key to species: Cult. AD1, G. hirsutum TM1; Wild AD1, G. hirsutum
Tx2094 from the Yucatan Peninsula; AD3, G. tomentosum WT936 from Hawaii; C1, G.
sturtianum C1-4 from Australia; Cult. A2, G. arboreum AKA8401; Wild A1, G. herbaceum
subsp. africanum (Watt) Vollesen from Botswana; D5, G. raimondii from Peru; D3, G.
davidsonii D3d-32 from Baja California; F1, G. longicalyx F1-3 from Tanzania; B1, G.
anomalum B1-1 from Africa.
at least one dispersal between Australia and Africa; another to the Americas,
which led to the evolution of the D genome diploids; and a second, much later
colonization of the New World by the A genome ancestor of the AD genome allopolyploids (see below).
Out of Africa, the Cytogenetic Center
of Diversity in the Genus (A, B, E, and F Genomes)
An important implication of the phylogenetic data for Gossypium is that it supports the proposition that Africa is the ancestral home for the genus (Fig. 2). This
is not strictly true from a purely cladistic standpoint, in that the basal phylogenetic split is between the New World and Old World diploids; however, the
supposition that Gossypium originated in Africa is supported by the genomic
Fig. 2. Biogeographic history of Gossypium. Following its likely origin 5 to 10 mya, Gossypium split into three major diploid lineages: the New
World clade (D genome); the African–Asian clade (A , B, E, and F genomes); and the Australian clade (C, G, and K genomes). The diversity of
genome sizes and seed morphologies in the genus are shown with exemplars from each genome group. See text for additional details.
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Taxonomy and Evolution of the Cotton Genus, Gossypium
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diversity found in the region (see below), versus the relative homogeneity found
in the New World. Fourteen species from Africa and Arabia are recognized in the
most recent taxonomic treatment of the genus (Fryxell, 1992) and together compose the African–Arabian subgenus Gossypium. Recognized within the subgenus
Gossypium are two taxonomic sections: section Gossypium, which contains four
subsections, and another African–Arabian section (Serrata), which contains the
single species G. trifurcatum Vollesen (found in desert area of eastern Somalia).
The presence of dentate leaves has raised the question of whether G. trifurcatum
belongs in the genus Gossypium at all, as dentate leaves are more characteristic
of Cienfugosia; however, molecular work has established that this poorly known
specimen is indeed a cotton species, if unusual in form (Rapp and Wendel, 2005).
This example underscores the provisional nature of much of the taxonomy of the
African–Arabian species of Gossypium, which are sorely in need of basic plant
exploration and systematic study. Other examples include subsection Pseudopambak, which contains several species whose recognition and definition are based
solely on limited herbarium material (e.g., G. benadirense Mattei, G. bricchettii
(Ulbr.) Vollesen, G. vollesenii). As no seeds have been collected and no living specimens are available, there exists no information on the cytogenetic characteristics
and molecular phylogenetic placement for these species. It is nearly certain that
new taxonomic diversity remains to be discovered in this region of the world.
Cytogenetically, the African–Arabian species are rather diverse and account
for four of the eight genome groups (A, B, E, and F), which neatly correspond to
their taxonomic subsections. The A genome group contains the two cultivated
cottons of subsection Gossypium, G. arboreum and G. herbaceum, while the three
African species in the B genome (G. anomalum Wawra, G. capitis-viridis Mauer, and
G. triphyllum) compose subsection Anomala. It bears noting that G. trifurcatum
(taxonomic section Serrata) may in fact belong to the B genome, but this has not
been established. The sole F genome species, G. longicalyx J.B. Hutch. & B.J.S. Lee,
represents subsection Longiloba, and, of the section Gossypium, it is considered
cytogenetically distinct (Phillips, 1966), morphologically isolated (Fryxell, 1971,
1992), and according to Fryxell may be better adapted to more mesic conditions
than any other diploid Gossypium species. Further adding to the interest in this
species is the phylogenetic placement of G. longicalyx as sister to the A genome
taxa (Fig. 2), which provides a window into the evolutionary origin of “long” fiber.
The remaining African–Asian species, those of subsection Pseudopambak, are considered to possess E genomes, although this has yet to be verified.
To Australia, with Genomic
Gigantism and New Ecological Specializations
Australia represents another center of diversity for the cotton genus. The Australian cottons (subgenus Sturtia) are represented by 3 taxonomic sections containing
17 total species, including one, G. anapoides J.M. Stewart et al., nom. inval., that is
newly described (Stewart et al., 2015). Cytogenetically, these taxa are divided into
the C, G, and K genome groups, having 2, 3, and 12 species, respectively. DNA
sequence data (Liu et al., 2001; Seelanan et al., 1997, 1999) support these groups
as natural lineages, consistent with their formal alignments into the taxonomic
sections Sturtia (C genome), Hibiscoidea (G genome), and Grandicalyx (K genome),
although the relationships among these three are yet unresolved. Some data
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Wendel & Grover
support a west to east radiation of Gossypium in Australia by placing G. robinsonii
F. Muell. (C genome) as the basal-most branch of the Australian clade (DeJoode
and Wendel, 1992). This basal placement of the C genome has not been observed
in the most recent analyses (Liu et al., 2001; Seelanan et al., 1997, 1999), which
provide no resolution among the Australian lineages and thereby highlight the
uncertainty in the phylogenetic history of the Australian cottons.
Taxonomically, the C and G genome groups are well understood, as these are
amply represented in collections and have been thoroughly studied (DeJoode and
Wendel, 1992; Fryxell, 1979, 1992; Liu et al., 2001; Seelanan et al., 1997, 1999; Tiwari
et al., 2014; Wendel et al., 1991). Species in the G genome are interfertile and apparently hybridize commonly (Tiwari et al., 2014; Wendel et al., 1991). The taxonomy
of the K genome (section Grandicalyx), however, is less certain. Collecting expeditions to the Kimberley region have doubled the number of recognized K genome
species in the past two decades through the discovery of at least seven new species (Fryxell, 1992; Stewart et al., 2015) and have expanded our understanding
of the diversity in this section. The species of this section are geographically,
morphologically, and ecologically distinct from other cotton species, frequently
exhibiting features characteristic of fire adaptation. Specifically, these are herbaceous perennials that exhibit a biseasonal growth pattern, where vegetative
growth dies back during the dry season and the plants survive as underground
rootstocks until fire or the return of the wet season initiates a new cycle of
growth. Also unique to section Grandicalyx are the flower and fruit morphologies.
K genome species possess upright flowers (like other cotton species) that subsequently become pendant following pollination. This change in floral positioning
is thought to aid in these uniquely ant-dispersed cotton seeds. That is, at maturity the pendant capsules release sparsely haired seeds, which bear elaiosomes
(fat bodies) that attract the ants who participate in their dispersal. Nearly all of
K genome species are poorly represented in collections (Campbell et al., 2010),
leading to much of this taxonomic uncertainty. These species have enormous
genomes, relative to others in the genus (Fig. 2), reflecting a relatively recent proliferation of gypsy-like transposable elements (Hawkins et al., 2006). Phylogenetic
analyses have yielded conflicting results regarding interspecific relationships in
section Grandicalyx (Liu et al., 2001; Seelanan et al., 1999), although there is some
support for a fundamental division of the section into a group of prostrate species
and a clade of more upright plants.
One final comment about the Australian species concerns their apparent
propensity to hybridize, a somewhat surprising observation given their present
status as species whose populations are mostly small, scattered, and geographically highly disjunct from those of related species. These geographical and often
phenological barriers notwithstanding, there is abundant evidence for multiple
episodes of historical introgression in the group, involving G. bickii Prokh., G.
sturtianum, and G. cunninghamii Tod. (Cronn and Wendel, 2004; Seelanan et al.,
1999; Tiwari et al., 2014; Wendel et al., 1991).
To the New World, Part I: The D Genome Diploids
A watershed moment in the evolutionary history of Gossypium followed a seemingly impossible transoceanic (either Atlantic or Pacific) dispersal of an African
ancestor to the shores of Central America, possibly on what is now the western
Taxonomy and Evolution of the Cotton Genus, Gossypium
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coast of Mexico. This dispersal event, dating to about 5 to 10 mya, led to the evolution and diversification of the New World D genome clade. This assemblage of
species have unusually small genomes for the genus (Fig. 2), due at least in part to
deletional clearance of much of the transposable element fraction (Hawkins et al.,
2009), and none bear spinnable fiber (Fig. 1). Taxonomically placed into subgenus
Houzingenia, the species are aligned into two sections and six subsections. These
species have been more thoroughly studied than most, and consequently their
taxonomy is reasonably well understood. Nonetheless, there remains sufficient
cryptic variability in the group that much remains to be learned about diversity
and relationships (Alvarez and Wendel, 2006; Cronn et al., 2003; Feng et al., 2011;
Ulloa et al., 2006, 2013; Wendel and Cronn, 2003; Wendel et al., 1995). This is particularly true for the “arborescent clade” comprising the group of small trees that
includes the widespread G. aridum (Rose & Standl.) Skovst. and the more narrowly distributed G. laxum L. Ll. Phillips, G. lobatum Gentry, and G. schwendimanii
Fryxell & S.D. Koch. Evidence indicates that cryptic variation exists within this
clade, possibly including new species related to G. aridum (Alvarez et al., 2005;
Feng et al., 2011) and G. laxum (Alvarez et al., 2005; Ulloa et al., 2006). There even
are populations of G. aridum from Colima that have a plastid genome much more
similar to those from G. klotzschianum (from the Galapagos Islands) and G. davidsonii (from Baja California) than to all other G. aridum populations, likely reflecting
historical interspecific gene flow (Alvarez and Wendel, 2006; Wendel and Albert,
1992). Gossypium gossypioides (Ulbr.) Standl. also has a somewhat mysterious introgressive ancestry (Cronn et al., 2003; Wendel et al., 1995), pointing out once again
the significance of ancient, natural interspecific hybridization in the generation of
diversity in the cotton genus (Cronn and Wendel, 2004).
The D genome cottons also have received considerable phylogenetic attention (Alvarez et al., 2005; Cronn et al., 2002, 2003; Feng et al., 2011; Ulloa et al., 2006,
2013; Wendel and Albert, 1992), which provides support for the naturalness of
most of the subsections. Evolutionary relationships among the apparently natural subsections are less certain, however (Alvarez et al., 2005; Ulloa et al., 2013),
although available evidence suggests that G. gossypioides is basal-most within
the subgenus (Cronn et al., 2003; Feng et al., 2011; Yu-xiang et al., 2013). All analyses support the monophyly of the arborescent clade, the grouping of the Baja
California species (G. harknessii Brandegee–G. armourianum Kearney–G. turneri
Fryxell) as a distinct clade, and the naturalness of the G. thurberi Tod.–G. trilobum
(DC.) Skovst. species pair, but the relative phylogenetic placements of these three
groups with G. raimondii Ulbr. remain uncertain.
Twelve of the 14+ D genome diploid species are endemic to western Mexico,
indicating this area is the center of diversity of the D genome. It seems likely, therefore, that this lineage became established and initially diversified in this region.
From this we can deduce later range extensions, probably relatively recently (during the Pleistocene), following long-distance dispersals leading to the evolution
of endemics in Peru (G. raimondii) and the Galapagos Islands (G. klotzschianum).
The latter species is closely related to G. davidsonii from Baja California, representing a clear and unusual case of this floristic connection (Wendel and Percival,
1990). As for G. raimondii, it is interesting that the sole South American representative of the New World diploid cottons is implicated as the closest ancestor of the
D genome of allopolyploid cotton (more on this below); the implication, perhaps
ironic, is that if allopolyploidy occurred in northern South America, as suggested
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(but not shown) by this observation, the possibility exists that they never would
have evolved had colonization of the New World by an A genome propagule not
followed closely on the heels of an earlier interhemispheric North American to
South American dispersal of the ancestor of what we now recognize as G. raimondii. This aspect of the origin of the allopolyploids makes an improbable story all
the more remarkable and yet again points to the recurring theme of the evolutionary significance of long-distance dispersal in cotton diversification.
To the New World, Part II: Origin and
Diversification of the Polyploid Cottons
A rich body of cytogenetic and experimental evidence now has demonstrated
convincingly that the tetraploid cotton species, which are entirely New World
in their distribution, are allopolyploids containing two coresident genomes: one
from an African or Asian A genome species and the other from a species similar
to the American D genome diploids (Endrizzi et al., 1985; Wendel, 1989; Wendel
and Cronn, 2003; Wendel et al., 2012). The hemisphere-scale allopatry of these two
diploid genome groups led to many decades of mystery surrounding the timing
and parentage of the New World allopolyploids. The question of “when” has been
convincingly addressed through gene sequence data that indicate allopolyploid
Gossypium originated approximately 1 to 2 mya in the mid-Pleistocene, before the
evolution of modern humans but relatively recently in geological terms (Flagel
et al., 2012; Senchina et al., 2003; Wendel, 1989). The question of parentage has
also been clarified through a wealth of DNA sequence data that indicate: (i) both
extant A genome species (G. arboreum, G. herbaceum) are equally distant from the
allopolyploid A genome and (ii) G. raimondii is the closest extant relative of the
actual D genome donor of the allopolyploid (Endrizzi et al., 1985; Li et al., 2014;
Wendel, 1989; Wendel and Cronn, 2003; Wendel et al., 2012; Yu-xiang et al., 2013).
Additionally, all allopolyploids contain an A genome cytoplasm, as evidenced
from analysis of both mitochondrial and plastidial genomes (Galau and Wilkins,
1989; Li et al., 2014; Small and Wendel, 1999; Wendel, 1989; Xu et al., 2012). Finally,
the studies mentioned above, and additional, multilocus DNA sequence data
(Grover et al., 2012), support a single origin for allopolyploid cotton.
As noted above, one truly remarkable feature of the origin of allopolyploid
cottons is that their genesis likely was dependent on the following series of highly
improbable events, which when considered in their totality amount to a biological marvel: (i) an ancient colonization of the New World by the ancestor of the D
genome diploids, following an initial transoceanic dispersal; (ii) a more recent
interhemispheric North American to South American dispersal of the ancestor
of modern G. raimondii; (iii) a third long-distance dispersal of an African–Asian
A genome ancestor to the New World, likely in the mid-Pleistocene; and (iv) the
chance biological encounter between the immigrant A genome taxon and the
endemic D genome entity, giving rise to hybridization and genome doubling, and
hence the genomic reunion among genomes that had been isolated on different
continents for 5 to 10 million years.
Given this now-justified scenario of a Pleistocene origin, the morphological diversification and spread of the allopolyploid cotton species must have been
relatively rapid following polyploidization. Classically, five allopolyploid species
were widely recognized, but a sixth species (G. ekmanianum Wittm.) was recently
Taxonomy and Evolution of the Cotton Genus, Gossypium
11
resurrected (Krapovickas and Seijo, 2008) and subsequently validated (Grover et
al., 2014) by molecular sequence data. In addition, ongoing studies provide justification for recognition of a seventh species that is relatively closely related
to G. hirsutum, from two islands (Wake, Peale) in the Wake Atoll in the Pacific
Ocean, Gossypium sp. nov. (J.F. Wendel, C.E. Grover, J. Jareczek, and J.P. Gallagher,
unpublished data, 2014). Included among the classically recognized species are
two island endemics, G. darwinii and G. tomentosum, that have differing population structures. Gossypium darwinii, a native of the Galapagos Islands, forms large
and continuous populations in some areas (Wendel and Percy, 1990), whereas
the Hawaiian endemic, G. tomentosum, tends to be more sparse, primarily occurring as scattered individuals and small populations on several islands. The latter
species, G. tomentosum, has recently received some attention with respect to its
reproductive biology and diversity (DeJoode and Wendel, 1992; Hawkins et al.,
2005; Pleasants and Wendel, 2010). A third classical allopolyploid, G. mustelinum
Miers ex G. Watt, is restricted to a relatively small region (Bahia state) of northeast
Brazil, where it survives in apparently relictual and highly homozygous scattered
populations (de Menezes et al., 2014; Wendel et al., 1994). In addition to these three
truly wild species, there exist two species with cultivated forms (G. barbadense
and G. hirsutum). Both species are characterized by large indigenous ranges that
in the aggregate encompass a wealth of morphological forms spanning the wildto-domesticate continuum (Brubaker et al., 1999; Brubaker and Wendel, 1993,
1994; Fryxell, 1979; Hutchinson, 1951, 1959; Hutchinson et al., 1947; Lubbers and
Chee, 2009; Percy and Wendel, 1990; Stephens, 1963). Gossypium hirsutum is widely
distributed in Central America and northern South America, the Caribbean, and
even reaches distant islands in the Pacific (Solomon Islands, Marquesas). Natural
diversity in this species is underscored by its complex nomenclatorial and taxonomic history (Fryxell, 1976, 1979). It is therefore unsurprising that a new species
from the Dominican Republic was recently discovered both in natural settings
and within the Gossypium germplasm collection (Grover et al., 2014; Krapovickas
and Seijo, 2008) and that other undescribed species likely are encompassed by the
diversity presently subsumed under the name G. hirsutum, as exemplified also
by Gossypium sp. nov., as noted above. Gossypium hirsutum has a more northerly
indigenous distribution than G. barbadense, with wild populations occurring as
far north as Tampa Bay, Florida (27°38¢ N) (J.M. Stewart, personal observation).
Gossypium barbadense has an indigenous range centered in the northern third of
South America but with a large region of range overlap with G. hirsutum in the
Caribbean (Percy, 2009).
Consideration of the ecological and geographic distribution of the allopolyploid species has led to the suggestion that polyploidy created the opportunity
to invade an ecological niche that is distinct from that occupied by most diploids. Fryxell (1965, 1979) noted that the truly wild forms of the allopolyploid
species typically occur in coastal habitats, in contrast to most of their diploid relatives. Three species (G. darwinii, Gossypium sp. nov., and G. tomentosum) are island
endemics that typically reside near coastlines, and two of the other species (G.
barbadense and G. hirsutum) possess wild forms that typically occupy littoral habitats tracing the Gulf of Mexico, northwest South America, and reaching distant
Pacific Islands. Fryxell speculated that the adaptations that allowed the newly
evolved allopolyploid to survive, and even thrive, in littoral habitats ultimately
facilitated the establishment of new polyploid species and provided a means for
12
Wendel & Grover
rapid dispersal of the saltwater tolerant seeds. These ideas gain additional support from recent ecological niche modeling studies (d’Eeckenbrugge and Lacape,
2014), which provide an elegant framework for understanding past and present
ecogeographic distributions of wild polyploid cottons.
Phylogenetic Relationships in the Genus
The genealogy of Gossypium has been evaluated by multiple molecular phylogenetic investigations (reviewed in Wendel and Cronn, 2003; Wendel et al., 2012),
each of which demonstrated that the major clades of species (i.e., genealogical
lineages) are largely consistent with geographical distributions, cytogenetic relationships (Baudoin et al., 2009; Endrizzi et al., 1985), and genome designations.
Thus, each taxonomically and cytogenetically established genome group corresponds to a single natural lineage, which also, in most cases, is geographically
cohesive. This information is summarized in a depiction of our present understanding of these relationships (Fig. 2 and 3).
Gossypium phylogenetic history has several broad aspects worth highlighting. First, four major diploid lineages exist that correspond to three continents:
Australia (C, G, and K genomes), the Americas (D genome), and Africa/Arabia
(itself containing two lineages: one comprising the A, B, and F genomes, and a
second solely containing the E genome species). Second, the earliest divergence
event separated the New World D genome lineage from that containing the ancestor of all Old World taxa, approximately 5 to 10 mya, making the New World and
Old World diploids phylogenetic sister groups. Subsequently, the Old World lineage itself diversified into three groups, namely, the Australian cottons (C, G, and
K genome species), the African–Arabian E genome species, and the African A, B,
and F genome cottons. Third, analyses identify the sole F genome species (G. longicalyx, Africa) as sister to the A genome clade (G. arboreum and G. herbaceum), where
the first emergence of fiber suitable for domestication evolved. This information
diagnoses the wild forms that best represent the ancestral lintless condition, and
provides a foundation for ultimately understanding the genetic basis of the origin of useful, long lint (cf. Fig. 2). Fourth, the major lineages of Gossypium are
characterized by rapid radiation and diversification that occurred shortly after
the genus originated and diverged from the Kokia–Gossypioides clade. Fifth, and
finally, the phylogenetic depiction summarizes our current understanding and
uncertainties regarding relationships among the seven allopolyploid species.
From Dispersal Ecology to Human Opportunity
As emphasized in this review, a consideration of the phylogeny of Fig. 2 and 3
in a temporal context leads to the realization that the genus has had an inordinate fondness for transoceanic travel. As already noted, this includes at least
one dispersal between Australia and Africa, another to the Americas (probably
Mexico) leading to the evolution of the D genome diploids, and a second, much
later, colonization of the New World by the A genome ancestor of the AD genome
allopolyploids. Long-distance dispersal played a role not only in diversification of
major evolutionary lines but also in speciation within Gossypium genome groups.
Examples include dispersals from southern Mexico to Peru (G. raimondii), from
northern Mexico to the Galapagos Islands (G. klotzschianum), from western South
Taxonomy and Evolution of the Cotton Genus, Gossypium
13
Fig. 3. Evolutionary history of Gossypium, as inferred from multiple molecular
phylogenetic data sets. The closest relative of Gossypium is a lineage containing the
African–Madagascan genus Gossypioides and the Hawaiian endemic genus Kokia.
Following its likely origin 5 to 10 mya, Gossypium split into three major diploid
lineages: the New World clade (D genome); the African–Asian clade (A, B, E, and F
genomes); and the Australian clade (C, G, and K genomes). This global diversification
involved multiple transoceanic dispersal events and was accompanied by
morphological, ecological, and chromosomal differentiation (genome sizes shown).
Interspecific hybridization has been exceptionally common during the evolution of
the genus. Allopolyploid cottons formed following transoceanic dispersal of an A
genome diploid to the Americas, where the new immigrant underwent hybridization,
as female, with a native D genome diploid similar to modern G. raimondii. Polyploid
cotton probably originated during the Pleistocene (1–2 mya), with the modern
species representing the descendants of an early and rapid colonization of the New
World tropics and subtropics.
America to the Galapagos Islands (G. darwinii), from Africa to the Cape Verde
Islands (G. capitis-viridis), and from the neotropics to the Hawaiian Islands (G.
tomentosum). What is so striking about this history is not just its biographically
fantastical nature, but also the lack of obvious adaptations for saltwater dispersal
14
Wendel & Grover
(Stephens, 1958, 1966). Not only that, but the life history bauplan for Gossypium is
of arid-zone adapted plants that one might assume at first blush do not possess
any capacity for overseas journeys. This aspect of the natural history of the cotton
genus represents a fascinating conundrum, one that lends itself more to speculation than to experimentation. Yet it also highlights the potential evolutionary
significance of the seemingly most improbable and rare events.
Given the absence of obvious adaptations for water dispersal, what can we
say about the evolutionary significance of the single-celled epidermal trichomes
for which cotton is justifiably so famous? The seeds and their coverings are
extraordinarily diverse in Gossypium, as illustrated in Fig. 1, which provides a
visual comparison of the various lineages of wild species and domesticated cotton species. Even though wild and cultivated cottons both produce fiber on the
seed coat, there are striking morphological and structural differences between
these fibers, the most obvious of which is their size. In contrast to the canonical (domesticated) cotton fiber, some D genome species (G. thurberi, G. trilobum,
G. davidsonii, and G. klotzschianum) do not possess obvious seed hairs; however,
the presence of these developmentally repressed structures is apparent under
microscopy (Applequist et al., 2001). Similarly, while the three D genome species
of subsection Caducibracteolata appear hairless to the unaided eye, these species
do in fact have seed hairs that are simply tightly appressed to the seed. Cultivated lint fiber is a model for cell wall developmental biology, as it is single cell
of almost pure cellulose that experiences remarkable elongation during development in cultivated species, achieving a final length up to 6 cm (Arpat et al., 2004;
Haigler et al., 2012; Kim and Triplett, 2001). In contrast, the wild-type fiber cell
is composed mostly of a combination of cellulose and suberin, which elongates
to <1 cm (Applequist et al., 2001; Haigler et al., 2009; Ryser and Holloway, 1985).
These and many other differences reflect both natural evolutionary processes
as well as human-mediated selection during domestication. The duration of the
elongation phase and the timing of onset of secondary wall synthesis appear to
be key determinants of the final length of the fiber in both wild and cultivated
plants (Applequis et al., 2001). Phylogenetic analysis of growth rates has shown
that the evolutionary innovation of prolonged elongation arose in the F genome/A
genome lineage, which may have facilitated the original domestication of the A
genome cottons. This trait of prolonged elongation was passed on to the allopolyploids, which in turn was a key component of their eventual domestication.
Relatively little is known about the developmental and genetic underpinnings of
the diverse morphologies illustrated in Fig. 2, but an improved understanding of
the changes that occurred during evolution and domestication may have implications for crop improvement (Hovav et al., 2007, 2008; Hu et al., 2013; Rapp et al.,
2010; Yoo and Wendel, 2014).
In nature, seed dispersal in Gossypium often follows a “shaker” model, where
erect, mature capsules dehisce along the sutures and the seeds are distributed
near the parental plant as wind shakes the branches. This likely is the ancestral
method of seed dispersal in the genus, as it occurs in all species of the B, C, E,
F, and (in part) D genome groups and in one species (G. bickii) of the G genome
group. The A, AD, (some) D, G, and K genome species have evolved other mechanisms of seed dispersal, with perhaps the most noteworthy innovation being the
fat bodies to facilitate ant dispersal on the seeds of the K genome species (Seelanan et al., 1999). The development of spinnable fibers apparently has occurred
Taxonomy and Evolution of the Cotton Genus, Gossypium
15
only once in the history of Gossypium, in the ancestor of the two A genome species
that became the progenitor of the A genome of the tetraploids.
The evolutionary “purpose” of epidermal seed hairs, or trichomes, is a matter of speculation. Fryxell (1979) suggested that elongated fibers aid dispersal by
birds, a hypothesis that gains credibility from sporadic mention of cotton seeds
in birds’ nests as well as a collection of G. darwinii from a finch’s nest in the Galapagos Islands (Wendel, unpublished data, 1990). One might also speculate that
fibers serve to inhibit germination unless there is sufficient moisture to saturate
the fibers; should germination occur following a light rain, there might not be
sufficient water for subsequent survival of the seedling. In this respect the waxy
coating of the fibers would repel water, to a point, and thus prevent premature
germination. A related possibility is that seed hairs function as “biological incubators” to facilitate germination only when ecological conditions are appropriate,
by recruiting particular microbial communities under appropriate moisture
regimes. Finally, two G genome species (G. australe, G. nelsonii) have evolved stiff
straight seed hairs that facilitate wind dispersal in that the stiffening hairs function to extrude seeds from the locules of the dehisced capsule.
It is against this natural history backdrop that ancient peoples discovered
that the unique properties of cotton fibers made them useful for ropes, textiles,
and other applications. This history has involved several cultures on different
continents and a parallel plant improvement process starting from divergent
and geographically isolated wild ancestors. Each of these crop species (G.
hirsutum, G. barbadense, G. arboreum, G. herbaceum) has its own history of domestication, diversification, and utilization (Brubaker et al., 1999; Hutchinson, 1951,
1959; Hutchinson et al., 1947; Lubbers and Chee, 2009; Percival et al., 1999; Percy,
2009; Percy and Wendel, 1990; Tyagi et al., 2014; Ulloa et al., 2013; Wendel et al.,
1992, 2009, 2010). Cotton domestication, thus, has been a replicated, and in many
respects parallel experiments for the four domesticated species. Many papers
describe various aspects of patterns of genetic diversity, the shape and severity of
genetic bottlenecks that accompanied the development of landraces and cultivars,
and the influence of recent human history on geographic patterns of cultivation
(Brubaker et al., 1999; Brubaker and Wendel, 1994, 2001; Fang et al., 2013; Hutchinson, 1951, 1954, 1959; Hutchinson et al., 1947; Percy and Wendel, 1990; Tyagi et al.,
2014; Wendel et al., 1989, 1992). It is worth reiterating that this history involved
human shaping and molding of naturally occurring diversity that originated
through the process of evolutionary diversification over a period of millions of
years, a legacy we continue to exploit today through deliberate introgression of
exotic germplasm from diverse, wild gene pools (Mehetre, 2010; Stelly, 2014; Wu
et al., 2010; Chapala et al., 2012; He et al., 2011a, 2011b; McCarty and Percy, 2001;
Nacoulima et al., 2012; Niles and Feaster, 1984; Zhang et al., 2011, 2014). Moreover,
new species of cotton and previously unrecognized taxonomic diversity continue
to be discovered today (Alvarez and Wendel, 2006; Feng et al., 2011; Grover et
al., 2014; Krapovickas and Seijo, 2008; Stewart et al., 2015; Ulloa et al., 2006), a
remarkable realization when one considers that Gossypium ranks among our most
important and hence frequently studied plant genera. The wild species of cotton,
consequently, represent an ample genetic repository for potential exploitation by
cotton breeders. The status of much of this diversity in the world’s germplasm
collections was recently reviewed (Campbell et al., 2010). Given current threats to
16
Wendel & Grover
global ecosystems, it has never been more critical than it is today to recognize this
legacy of speciation and diversification for humankind.
Acknowledgments
Research in the Wendel lab has largely been funded by the NSF Plant Genome Program,
with additional support from other NSF programs, the USDA NRI, and Cotton Incorporated.
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