The Evolution of Regional Species Richness - The Theory of The Southern African Flora

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Species Richness: The History
of the Southern African Flora
Annu. Rev. Ecol. Evol. Syst. 2015.46:393-412. Downloaded from www.annualreviews.org
Access provided by University of Nebraska - Lincoln on 12/04/15. For personal use only.
H. Peter Linder1 and G. Anthony Verboom2

1
Institute of Systematic Botany, University of Zurich, CH-8008 Zurich, Switzerland;
email: peter.linder@systbot.uzh.ch
2
Department of Biological Sciences, University of Cape Town, 7701 Rondebosch,
South Africa; email: tony.verboom@uct.ac.za
Annu. Rev. Ecol. Evol. Syst. 2015. 46:393–412 Keywords

The Annual Review of Ecology, Evolution, and angiosperm, biodiversity, diversification, Cape flora, Cenozoic, nested
Systematics is online at ecolsys.annualreviews.org
radiations
This article’s doi:
10.1146/annurev-ecolsys-112414-054322 Abstract
Copyright c 2015 by Annual Reviews. The flora of southern Africa is, for its latitude and area, very species-rich.
All rights reserved
Although the hyperdiverse Cape flora contributes almost half of this rich-
ness, three other radiations (desert, grassland, and woodland) contribute
significantly to the botanical wealth of southern Africa. Each radiation oc-
curs in a different ecological setting and has a different diversification his-
tory. Such parallel radiations can develop in suitably complex environments,
given gradual change through time and no region-wide catastrophes. These
four radiations cross-seeded each other, with clades spawning subclades in
other radiations, thus linking all four into one complex radiation. This led
to an increase in the number of diversifying clades in each radiation. Such
complex radiations accumulate diversifying lineages over a long time, spawn
daughter radiations on other continents, and become powerhouses of global-
biodiversity generation. We suggest that several of the most species-rich
regions may harbor such complex radiations.
393
INTRODUCTION
It has long been appreciated that diversity is unevenly distributed across the planet. Mutke &
Radiation: a general Barthlott (2005) showed that plant-species diversity is regionally concentrated, being highest
term referring to an in the northern Andes, the South American Atlantic forests, southern Africa, the southeastern
increase in either Himalaya, and Southeast Asia. High diversity is invariably generated by evolutionary radiation,
taxonomic or trait
which is, however, a feature of individual lineages. A sophisticated research program has developed
diversity, or both, in a
lineage to test for shifts in the rate of diversification within lineages, to determine whether such shifts reflect
accelerated speciation or reduced extinction (e.g., Alfaro et al. 2009, Morlon et al. 2011, Rabosky
Floristic radiation
(FR): 2014) and to assess which traits or events might explain them (FitzJohn 2010, Maddison et al.
radiations in several 2007, Silvestro et al. 2013). Where multiple lineages making up a regional biota have radiated,
phylogenetically it is not uncommon to speak of the radiation of a flora or a biota (Crisp et al. 2004, Linder
independent clades 2003), and we refer to this as floristic radiation (FR). The evolution of regional richness has been
within a predefined
investigated in several regions (Linder 2008), notably the biota of the Amazon basin (Hoorn et al.
flora
2010) and the tropical Andes (Saerkinen et al. 2012), the New Zealand flora (Winkworth et al.
Complex radiation:
2005), the Australian flora (Crisp & Cook 2013), and the Cape flora of southern Africa (Linder
several floristic
radiations in a larger 2003; Verboom et al. 2009, 2014).
region that mutually A frequent implicit assumption of such studies is that the individual lineage-specific radiations
seed each other with share a common cause and timing. The most spectacular such singular event is, perhaps, the
further lineages that Andean orogeny linked to the radiation in the páramo (Hughes & Eastwood 2006, Linder 2008,
radiate
Madriñán et al. 2013). Mountain building has also been implicated in the FR of New Zealand
(Heenan & McGlone 2013) and in the Himalaya (Wen et al. 2014). Evidence is accumulating,
however, that in at least some systems high regional diversity might be the consequence of a more
complex and differentiated process. The diversity of the northern Andean flora, for example, is
likely the product of several distinct processes stimulating the radiation of its Andean and lowland
components (Antonelli et al. 2009, Hoorn et al. 2010, Saerkinen et al. 2012). We argue that the
radiation of a regional flora might constitute a set of nested radiations in which the geographically
and ecologically separated radiations seed each other, thus spawning daughter radiations, and
so increasing the total number of diversifying clades. This process might be most common in
the context of spatially separated radiations, but may also occur between temporally separated
radiations in which one radiation provides the lineages that fuel the next (replacement) radiation.
It could be argued that only such composite processes can lead to the extraordinarily high peaks of
regional diversity found in the northern Andes, the eastern outliers of the Himalaya, the Indonesian
islands, and the Cape region.
Complex radiations most likely occur in regions characterized by specific environmental con-
ditions (geomorphological and climatic). First, environmental complexity, typically involving a
close juxtaposition of contrasting environmental conditions, is required to host multiple parallel
FRs. Under these conditions it is possible for FRs in one environment to be seeded from radi-
ations taking place in the other environments. Such a situation is found in the northern Andes,
which has closely juxtaposed rainforest, montane forest, dry tropical forests, tropic–alpine, and
desert environments. Second, general, or at least local, environmental stability, particularly the
absence of vegetation-obliterating cataclysms, is important in enabling the products of radiation
to persist. Examples of diversity-obliterating cataclysms include the Quaternary alternation of ice
sheets (e.g., in Northern Europe), flooding of low-lying epicontinental regions (e.g., by the North
Sea or Java Sea), and extreme aridification (e.g., in the Sahara). Finally, moderate, localized, or
gradual environmental change might stimulate complex radiations, both by facilitating turnover,
and so fostering evolutionary dynamism, and by providing local regions within which new FRs
can be started.
394 Linder · Verboom

Complex radiations should generate a distinctive macroevolutionary signature, enabling them

to be diagnosed via an analysis of their phylogenetic pattern. First, we predict that at least some
of the lineages should show nested radiations, in which radiations in one environment seed nested
radiations in an adjacent environment. Second, because the extrinsic or environmental triggers
for radiation are temporally staggered, the radiations should not start simultaneously. Instead,
the timing of radiations will be staggered, reflecting both the times of the appearance of alterna-
tive environmental conditions and the time taken by lineages to occupy the new environments.
Finally, we predict that lineages that radiate taxonomically and morphologically, and especially
lineages that are part of complex radiations and so radiate in diverse habitats, are more likely to
experience successful long-distance dispersal to other regions. Regions with complex radiations
could therefore contribute substantially to extraregional diversity.
SOUTHERN AFRICA AS AN EXAMPLE
Richness
With approximately 22,755 species and subspecies (Klopper et al. 2007), the southern African
flora ranks among the richest temperate and subtropical floras globally, when latitude and area
are taken into account (Figure 1). It is ecologically separated from the rest of the continent by
the ancient, wide Limpopo River valley and the Kalahari Desert, and is biogeographically distinct
from tropical Africa (Linder et al. 2012), with approximately 78% species-level endemism. At a
higher taxonomic level, the southern African flora is African. The arid flora of the Kalahari is
related to that of northwest Africa, forming the arid corridor (Bellstedt et al. 2012, de Winter
1966, Thiv et al. 2011); the savannas are a southern outlier of the Zambezian savannas (White
1983); and the temperate grasslands are associated with the upland floras of tropical Africa (Galley
et al. 2007, Linder 2014), forming the Afrotemperate distribution pattern (Linder 1990).
4.6
4.4 sa
me us
in
Log species richness
4.2 au
4 ar
pa ir
3.8
it
gr sp
3.6 ch
mo
al
3.4 nz
ur
3.2
3
5 5.5 6 6.5 7 7.5
Log area (km2)
Figure 1
Species richness of southern Africa (sa) compared with the floras of other countries at approximately the same
latitude. Countries above the fitted line are more species-rich than expected, and below the fitted line they
are less so. Species-richness values for each country are from Heywood & Davis (1994) (see Supplemental Supplemental Material
Table 1; follow the Supplemental Material link from the Annual Reviews home page at http://www.
annualreviews.org). Abbreviations: al, Algeria; ar, Argentina; au, Australia; ch, Chile; gr, Greece; in, India;
ir, Iran; it, Italy; me, Mexico; mo, Morocco; nz, New Zealand; pa, Paraguay; sa, southern Africa; sp, Spain;
ur, Uruguay; us, United States.
www.annualreviews.org • Evolution of Regional Species Richness 395

o
pop
Lim
Desert
Woodland FR
FR Kalahari
1
Na
mi
6 Highveld
b
Grassland
Orange River FR
Na
Nama Karoo
g
ma
er
i ii
sb
s
qu
nd
en
Be
iii Kamiesberg
la
ala
ak
ng
id
Dr
nd
lM
ue
ta
la
Na
ants 5
Olif ver 2
>2,000 Ri
1,500–2,000
1,000–1,500 Fynbos FR nt
500–1,000 iv re
0–500 Cur 0 50 100 200
Cape Fold 3 as
Elevation (m) vi lh Scale
v Mountains Port
Agu
Elizabeth
Atlantic Ocean Indian Ocean
Cape Agulhas
Figure 2
Southern Africa with the main topographic features mentioned in the text labeled. The spatial centers of the
four radiations are encircled. The arrows indicate seeding events: Thick lines indicate more than 10 seeding
events; medium lines indicate 5–10 seeding events; and thin lines indicate fewer than 5 seeding events. The
illustrations show typical clades spawned into the receiving radiation: () Diascia barberae (Scrophulariaceae),
() Disa uniflora (Orchidaceae), () Penaea mucronata (Penaeaceae), () Gladiolus floribundus (Iridaceae),
() Nerine mansellii (Amaryllidaceae), and () Delosperma cooperi (Aizoaceae). Fossil sites are indicated with
blue triangles: (i ) Noup, (ii ) Arnot, (iii ) Koingnaas, (iv) Langebaanweg, (v) Noordhoek, and (vi ) Knysna.
Paleoenvironments
Southern Africa (Figure 2) has had a remarkably uneventful Cenozoic environmental history
(Table 1). Since the Cretaceous, the geomorphology of the region has been dominated by a high
central plateau and narrow coastal plain, separated by a marked escarpment (but see Neumann &
Bamford 2015, who suggest that the subcontinent was completely peneplained in the Paleogene).
The only changes have been those precipitated by two uplift events that raised the eastern part of
the subcontinent relative to the west, thus contributing to the establishment of the modern alpine
environments along the highest parts of the eastern escarpment (known as the Drakensberg).
Benguela Upwelling
Climatic change, probably driven by the glaciation of neighboring Antarctica, was mostly toward
System: the upwelling
of cold water along the increasing aridity and seasonality. This change culminated in the establishment of summer-dry
Atlantic coast of conditions along the western coastal region. At the subcontinental level, climate change was proba-
southern Africa that bly moderated by topography, with the high elevations retaining cooler, and so effectively moister,
brings Antarctic environments. Consequently, it is likely that the geomorphological structure of the subcontinent
meltwater to the
and the global position between the warm Agulhas Current in the Indian Ocean and the cold
surface
Benguela Upwelling System in the Atlantic Ocean led to the triple combination of environmental
complexity (coastal plains and central plateau), stability, and local, gradual change.

Table 1 Summary of the environmental history of southern Africa

Era Geomorphology Climate
Setting the Southern Africa contains some of the oldest continental
scene rocks (the Kaapvaal Craton). The Cape Supergroup
was deposited into the Agulhas Sea along the southern
margin of this craton during the first half of the
Paleozoic; mountain folding started during the
Carboniferous, followed by erosion northwards to form
the Karoo Supergroup (Late Carboniferous to Middle
Jurassic) (McCarthy & Rubidge 2005). During much of
the Paleozoic and Mesozoic periods, southern Africa
was embedded in the center of Gondwana.
Late Southern Africa separated from Western Gondwana as a Cretaceous climates in southern Africa may have been
Cretaceous 1,500 m plateau, with an emergent Lesotho plateau at wet (Tyson &Partridge 2000). In addition, climates on
2,400 m, and the continental margins forming a high the plateau would have been relatively cool due to the
escarpment (Partridge & Maud 2000). Subsequent elevation.
erosion rapidly drove the escarpment inland,
differentiating a coastal and an inland peneplain. This
resulted in the exhumation of, inter alia, the Cape Fold
Mountains and the Kamiesberg range (Partridge &
Maud 2000).
Paleocene By the beginning of the Paleocene, the Cape Fold Some aridity developed, as inferred from the formation
Mountains were isolated on the coastal plain. Erosion of silcretes (Tyson & Partridge 2000) but the Namib
rates had slowed (Tinker et al. 2008a, Tinker et al. was humid (Pickford et al. 2014).
2008b), resulting in little geomorphological change
during the Cenozoic. The Cape Fold Mountains
retained a juvenile structure, possibly due to the
erosion-resistant sandstones (Scharf et al. 2013). The
coastal peneplain (often with duricrusts) and inland
plateau persisted, separated by the escarpment edge.
Eocene Semiarid conditions developed in the Namib during the
Late Eocene (Pickford et al. 2014).
Oligocene The global climate was probably cooler and more arid
than the Late Eocene, this climate change is associated
with the glaciation of Antarctica (Dupont-Nivet et al.
2007); semiarid conditions persisted in the Namib
(Pickford et al. 2014).
Early Miocene Uplift of 250 m along the eastern edge of the central Namaqualand had a tropical-to-subtropical wet climate;
escarpment, with less uplift in the west, resulted in the Orange River Valley was wooded; and the Namib
peneplanation down to the Post-African I surface, and was probably semiarid (Senut & Segalen 2014). The
an increase in the steepness of the western drainage. hyperarid Namib climate probably originated
The resulting peneplain was armored with a duricrust approximately 17–16 Ma ago (Senut et al. 2009).
(silcretes).
Middle Deep-sea cores taken from along the West Coast
Miocene indicate an increased upwelling of cold Benguela waters
and the establishment of a drier climate (Dupont et al.
2011, Dupont et al. 2013, Hoetzel et al. 2013). This
accentuated the east–west aridity gradient. Comparable
evidence is lacking from the eastern side of the
subcontinent and from the central plateau.
(Continued )

Table 1 (Continued )
Era Geomorphology Climate
Late Miocene The longitudinal aridity gradient was further
accentuated by the strengthening of the eastern warm
Agulhas Current and western cold Benguela Upwelling
(Siesser 1980), and there is further evidence of a winter
rainfall regime in the west (Dupont et al. 2011).
Pliocene Uplift centered on the Natal Midlands (250–300 km A brief humid period during the Pliocene resulted in the
inland) resulted in an elevation increase of 700–900 m. rejuvenation of several inland rivers (Tyson &
The elevation of the uplift decreased in all directions Partridge 2000).
from the epicenter, and along the West Coast it was
only 90–110 m (Partridge 1998). The erosion rate of
the Post-African I surface was among the slowest
globally (Bierman et al. 2014). Much of the erosion was

due to river incision, which resulted in a more dissected
landscape. The limestone coastal plain in the southern
Cape was exposed.
Pleistocene Fluctuating sea levels led to the repeated exposure of an Glacial conditions on the Drakensberg were probably
extensive coastal plain in the southern Cape at Cape colder and associated with small glaciers (Mills et al.
Agulhas. 2009); it has been suggested that there were wetter
conditions along the West Coast (Parkington et al.
2000) and drier conditions along the southern Cape
coast (Barrable et al. 2002).
Conditions are described when they change, and they are not repeated if they remain constant between eras.
Radiations
Linder (2008) and Verboom et al. (2014) have argued that the richness of the Greater Cape flora
is the product of distinct radiation scenarios affecting the montane fynbos flora and the succulent
flora of the western coastal margin. Here, we argue that this pattern is true of the broader southern
African flora. We postulate four FRs occurring within southern Africa. We refer to these as the
Fynbos, Desert, temperate Grassland, and tropical Woodland FRs. We predefine these FRs on
the grounds that we expect them to differ in terms of their geographic centers, ecology, starting
times, and diversification rates. However, we are aware that this is a simplification, and that several
of these FRs, on more detailed inspection, may be considered as composite (Bergh et al. 2014,
Verboom et al. 2014).
The Fynbos FR is centered at the southwestern tip of the subcontinent, on the mountain ranges
and intermontane valleys of the coastal plain, from Port Elizabeth to the Olifants River (Figure 2).
Fynbos: heathy It associates predominantly with the highly dystrophic soils derived from the weathering of the
vegetation of finely
Cape Fold sandstones, and is influenced by a predominantly winter-wet summer-dry climate. Fires
branched evergreen,
sclerophyllous are a regular feature of this system, mostly occurring every 10–20 years (Kraaij & Van Wilgen
fine-leaved shrubs, 2014). The product of the Fynbos FR is often referred to as the Cape flora, although this term has
dominated by also been used by, among others, Goldblatt (1978) and Manning & Goldblatt (2012) to include
Proteaceae, forest, thicket, and succulent karoo lineages, the evolutionary histories of which differ strikingly
Restionaceae, and
from those of fynbos lineages (Bergh et al. 2014, Verboom et al. 2014). The Cape flora is rich, with
Ericaceae, and
restricted to more than 10,000 species (Manning & Goldblatt 2012), more than half of which are derived from
oligotrophic soils just 30 major radiations (Linder 2003). Among the best known are the radiations of Iridaceae,
Restionaceae, Proteaceae, and Erica. Whereas the oldest clades date to the Late Cretaceous or
Paleogene [e.g., Bruniaceae (Quint & Classen-Bockhoff 2008)], most radiations date to the Late

Eocene, Oligocene, and Miocene (Verboom et al. 2014). However, the modern diversity of at
least some lineages arose in the last 10 million years [e.g., Muraltia (Forest et al. 2007)], and some
clades were first added in the Pliocene [e.g., Heliophila (Mummenhoff et al. 2005)]. It seems most
Succulent karoo:
likely, therefore, that the bulk of modern species diversity has been generated since the Middle low vegetation mostly
Miocene. It is not clear, however, whether this recent origin of the extant diversity is due to Late dominated by leaf-
Miocene turnover in a flora that had been diverse since the middle of the Cenozoic or whether succulent shrubs
the region was previously less species-rich. belonging to the
Aizoaceae and
The Desert FR is centered in the Namaqualand and Namib regions, on the western escarp-
Crassulaceae, and rich
ment and coastal plain of southern Africa. It associates with strongly summer-arid conditions, in annual and
and the Benguela Upwelling System and associated atmospheric circulation systems dictate a geophytic species
strictly winter precipitation regime (Mucina et al. 2006b). Although it is, broadly, a general desert-
environment radiation, its most spectacular manifestation is the radiation of the succulent karoo
flora in the summer-dry semiarid desert. Floristically, this radiation is characterized by the explo-
sive diversification of succulent lineages, notably Aizoaceae and Crassulaceae (Klak et al. 2004).
For a semiarid environment, the flora is spectacularly rich (Cowling et al. 1998), with some 3,500
species (Snijman 2013). Phylogenetic data have identified most succulent karoo-endemic lineages
as originating after the Middle Miocene (Verboom et al. 2009), whereas both molecular and fos-
sil data have identified the ruschioid Aizoaceae as radiating during the Pliocene (Dupont et al.
2011, Klak et al. 2004). The succulent karoo FR is, however, nested within a much more widely
distributed and probably much older desert system that reaches northwards to Angola and inland
to Botswana. This broader desert system likely provided an arena for the early diversification of
Scrophulariaceae and possibly Crassulaceae.
The temperate Grassland FR is centered on the eastern escarpment and the high plateau
adjacent to this, often referred to as the Highveld. It is characterized by mild, wet summers; cold,
dry winters; and annual or biennial fire (Mucina et al. 2006a). The characteristic taxa include grasses
(Danthonioideae), terrestrial orchids (Orchidoideae), Hyacinthaceae, Kniphofia (Asphodelaceae),
and Apocynaceae. Many of these clades are widespread in the Afromontane grasslands, reaching
north to the Ethiopian plateau and westwards to the headwaters of the Niger at Fouta Djallon.
The grassland is often associated with patches of laurophyllous forest. Nested in this Grassland
radiation is an alpine FR geographically restricted to the plateaus and peaks of the Drakensberg and
the Maluti, at elevations above approximately 1,800 m, which accommodates some 2,200 species
(van Wyk & Smith 2001) and is known as the Drakensberg Alpine Center (Carbutt & Edwards
2006). In this alpine zone the cold is more extreme, often with frost and snow, and the fire frequency
is lower. The alpine system is probably much more recent than the rest of the grassland, dating to
the Pliocene, when the most recent uplift elevated the eastern plateau to approximately 3,000 m.
Typical radiations in the alpine include Scrophulariaceae (e.g., Glumicalyx), Asteraceae (especially
Helichrysum), Hypoxidaceae (Rhodohypoxis), Campanulaceae (Craterocapsa), and Ericaceae (Erica).
The tropical Woodland FR is associated with wetter sites along the eastern escarpment and
coastal plain of the subcontinent, and with a savanna on the northern slopes of the central plateau.
This radiation includes laurophyllous Afromontane forest, tropical forests, savanna and thicket
vegetation, and the associated edaphic grasslands. The environments occupied by this FR are
mesic, frost-free and dominated by summer precipitation (Mucina & Rutherford 2006). The
evolutionary dynamics of the southern African woodland flora remain poorly studied. Important
families include Fabaceae [e.g., Acacia (Mimosoideae)], Combretaceae, Euphorbiaceae, Rubiaceae,
Malvaceae, Sapindales, and Celastraceae. There is a small radiation of southern African epiphytic
orchids (Mystacidium) associated with the forests, and the edaphic grasslands contain the large
orchid genus Eulophia. Although there appear to be no large radiations in this system within
southern Africa, it may have had a long history within the region.

Table 2 Major Cenozoic fossil sites in southern Africaa

Site name Age Region Reference(s) Notes
Arnot Paleocene Namaqualand Scholtz 1985 Both woodland and fynbos elements
Koingnaas “Tertiary” Namaqualand de Villiers & Cadman 2001 Podocarpus, woodland; possibly early
Cenozoic
Knysna Miocene–Eocene Southern Cape Phillips 1927, Thiergart et al. Scott (1995) interpreted this as a
lignites 1963, Thwaites & Jacobs 1987 restioid swamp in proteoid
woodland
Langebaanweg Middle Miocene Southern West Coetzee & Rogers 1982 Tropical elements along a
Coast meandering river
Noordhoek Early and Late Cape Peninsula Coetzee 1983, 1986 Upper layers of typical fynbos
Miocene elements, resting unconformably
on layers with austral temperate
forest elements
Atlantic Late Miocene Namibian West Dupont et al. 2011, 2013; Hoetzel Documenting the vegetation
offshore Coast et al. 2013 development of the West Coast to
Angola: tropical grassland replaced
by arid and fynbos elements
during the Late Miocene
Noup Miocene? Namaqualand Scott 1995 Podocarpus, Olea, Proteaceae,
Myrtaceae (woodland and forest)
a
Isolated finds of wood and pollen are not included. The sites are mapped in Figure 2.
Paleobotanical Evidence
The southern African fossil record is frustratingly poor and geographically biased (Table 2 and
Figure 2, Neumann & Bamford 2015), yet it is consistent with some interpretations. All onshore
deposits contain pollen from trees or wood, indicating a widespread presence of woodland or
forest until the Miocene. The pollens suggest that these Cenozoic forests were different from the
modern laurophyllous forests. All three major sites (Arnot, Noordhoek, and Knysna) contained
Podocarpaceae, Chloranthaceae, Casuarinaceae, Proteaceae, and Cornaceae. Araucariaceae has
been found only at Arnot; Sarcolaenaceae has been found at both Knysna and Noordhoek (Nilsson
et al. 1996); and Winteraceae has been found only at Noordhoek (Coetzee & Praglowski 1988).
Of this list, Winteraceae, Sarcolaenaceae, Casuarinaceae, and Chloranthaceae are now extinct in
continental Africa. Comparable forests are still found in Madagascar (Nilsson et al. 1996). This
suggests that with Neogene aridification, the forests were not only massively reduced in extent and
restricted to local mesic habitats, but that the diversity was also dramatically reduced. Until the
Late Miocene, Podocarpus forests remained quite widespread, with pollen of indicator taxa being
found offshore of the mouth of the Orange River (Dupont et al. 2013) as well as onshore in undated
deposits from Namaqualand (Podocarpus, Olea, Proteaceae, and Myrtaceae) (Scott 1995). These
Podocarpus-dominated forests are characteristic of the extant laurophyllous Afromontane forests.
Fynbos clades have been reported from most southern African fossil sites throughout the
Cenozoic. Although there are no Cenozoic fossils situated on the sandstone mountains proper,
these environments form the present-day stronghold of fynbos lineages, and it seems likely that
they were occupied by fynbos lineages throughout the Cenozoic.
There is ample zoological evidence of a semiarid proto-Namib from the Late Eocene (Senut
et al. 2009), and botanical evidence indicates a further round of aridification from the Late Miocene.

Cores from offshore deep-sea drilling have documented the increasing dominance of Aizoaceae,
a typical element of the succulent karoo FR, during the Late Miocene to Early Pliocene (Dupont
et al. 2011), and the expansion of arid-adapted taxa in the Namibian interior during the latest
Pliocene (Dupont et al. 2013, Hoetzel et al. 2013). Isotope ratios in fossil ratite eggshells confirm
that the modern balance of a winter-versus-summer rainfall desert has existed at least since the
Miocene (Segalen et al. 2006). Whereas climatic reconstructions suggest semiarid conditions
existed along the West Coast from the Late Eocene, the pollen record suggests a Late Miocene
to Early Pliocene initiation of the Desert FR.
As there are no Cenozoic fossil sites from the central plateau of southern Africa, offshore pollen
cores (Dupont et al. 2013, Hoetzel et al. 2013) constitute the only line of paleobotanical evidence
giving insights into the emergence of the grassland and alpine floras. These data suggest an initial
appearance of grassland in the Middle Miocene, with grasslands replacing Podocarpus forests by the
Pliocene in association with increased fire and a transformation of C3 grassland to C4 grassland.
PREDICTED PATTERNS OF RADIATIONS
Staggered Radiations
In order to date and compare the initiation and the progression of the FRs, we compiled phy-
logenetic data for all clades that could be assigned to a particular FR, and for which molecular
crown-age estimates are available, and that have at least two species in that particular FR (Sup- Supplemental Material
plemental Table 2 and Figure 3). As predicted for a complex radiation, this revealed no single
starting time, and a continuous accumulation of radiating lineages in the southern Africa radiation.
At least one lineage in each of the four FRs dates back to the Eocene, suggesting that this range
of habitats (oligotrophic soils for the Fynbos FR, semiarid conditions for the Desert FR, cool
mesic conditions for the Grassland FR, and warm mesic conditions for the Woodland FR) has
existed throughout the Cenozoic in southern Africa. However, the very small number of clades
suggests that caution should be used in the interpretation. From the Middle Eocene the FRs show
accelerated accumulation of radiating clades in the following sequence: Desert I (Middle Eocene),
Fynbos (Late Eocene), Grassland (Early Oligocene), and, finally, Desert II (Late Miocene). Due
to the small number of dated Woodland clades, the history of the Woodland FR remains obscure.
All radiations (except Desert I) continued recruiting lineages once started, and we suggest that
Desert I was largely replaced by the Desert II FR following the increased proportion of winter
rainfall that occurred from the Late Miocene.
We tentatively propose initial environmental conditions for these FRs. Our geomorphological
interpretation suggests that the oligotrophic habitat occupied by the Fynbos FR has been available
since the beginning of the Cenozoic. This implies an unexplained 30 million year lag time prior
to the initial radiation of the flora, and we suggest that the increased seasonality and aridity of
the global Late Eocene–Early Oligocene may have provided suitable conditions for the expansion
and radiation of fynbos heathland. A similar explanation might be made for the Early Oligocene
Grassland FR. Although termed the Grassland FR, the key factor enabling the initial development
of this system was likely the availability of open habitats in an otherwise forested landscape. These
open habitats might have been transformed to grassland during the Miocene, leading to a second
increase in the number of crown groups in the Grassland FR in the Late Miocene–Early Pliocene.
The Desert I FR coincides with the establishment of semiarid conditions in the Late Eocene
Namib. The Desert II FR is in the succulent karoo, and is linked to the establishment of summer
drought in this semiarid region (Dupont et al. 2011).

Table 3 The number and direction of seeding events in which a clade in one floristic radiation (FR)
Supplemental Material (the source) spawns a subclade in another FR (the sink), summarized from Supplemental Table 3
Sink FR
Source FR Fynbos Desert Grassland Woodland Total
Fynbos – 10 (1.4–11.3) 11 (3.3–25) 0 21
Desert 4 (1–6) – 4 (4–6) 0 8
Grassland 6 (10–30) 3 (3.4–30) – 1 9
Woodland 3 (8–23) 0 0 – 3
Total 13 13 15 1 42
The first value in a cell is the number of clades with such seeding events: Even though there may have been several seeding
events per clade, they were counted only once. The range of median ages for these seeding events, in millions of years, is
given in parentheses.
Nested Southern African Patterns

If the southern African FRs were to constitute a complex radiation, then there should be ev-
idence that at least some FRs were seeded from other southern African FRs. We expect that
three factors might control the direction and the frequency of dispersal. First, older radiations
have more opportunity to seed younger radiations than vice versa, and this might primarily im-
pact the direction of the seeding. Second, we expect that species-rich radiations are more likely
to spawn daughter radiations than those that are species-poor. And, finally, habitat compatibility
most likely influences which transitions are possible. The last two factors might primarily influ-
ence the number of seeding events. To examine this idea, we compiled phylogenetic data for all
clades that have subclades in at least two radiations and for which a phylogenetic hypothesis was
available. We assigned the tips to southern African biomes or, if from outside southern Africa,
to continents, and used dispersal–vicariance analysis optimization (Ronquist 1997) to infer the
ancestral biomes or continents and the descendant biomes or continents. The detailed results are
shown in the Supplemental Materials.
The Woodland FR has spawned just three daughter radiations, all in the Fynbos FR, and it has
received only one lineage from the other FRs (Table 3, Figure 2, and Supplemental Table 3).
Although this might be taken as evidence of the youth of the Woodland flora, the fossil record
identifies woodland and/or forest as potentially the oldest vegetation formations in southern
Africa. Consequently, its failure to seed other radiations is surprising. Although numerous
Woodland clades have species in the desert or grassland, these did not radiate. This is exemplified
by Mimosoideae, with a southern African Woodland radiation dated to approximately 14.6 Ma
(Bouchenak-Khelladi et al. 2010), and with only the well-known camelthorn (Acacia erioloba)
endemic along watercourses in the arid areas. Woodland taxa are also often found in grassland,
but as small patches of forest often dominated by Podocarpus.
The Fynbos FR contributed more than twice as many lineages to other radiations than did the
next most productive radiation, the Grassland FR. More or less equal numbers of lineages were
spawned from the Fynbos FR in the Grassland and the Desert FRs (Table 3). Moreover, many
clades show repeated spawning events, so the true number is much larger than that indicated here.
Some clades spawned radiations only in the Grassland (e.g., Protea, Restionaceae), but most appear
to have daughter radiations in both the Desert and Grassland FRs. There are several explanations
for the dominant source-role of the Fynbos FR. One is that it is older than the Desert or the
Grassland FRs (Figure 3) and so is more likely to be a source for the seeding of younger radiations.
A second is that the Fynbos FR is very species-rich, with more than twice as many species as the next
largest radiation, which implies a greater number of lineages that could potentially invade other

12
Plio–Pleistocene
Paleocene
Eocene Oligocene Miocene
10
Number of crown radiations

8
6
2
Desert I
Desert II
0
60 55 50 45 40 35 30 25 20 15 10 5 0
Time (millions of years)
Desert Fynbos Grassland Woodland
Figure 3
Dating the initiation and the progression of the four floristic radiations (FRs) in southern Africa, based on the crown ages of the clades,
as summarized from Supplemental Table 2. Clades from all four radiations were already present during the Eocene. The first increase
in the number of diversifying lineages occurred during the Late Eocene Fynbos FR, which is followed in the Oligocene by the
Grassland FR and in the Miocene by the Desert II FR.
systems. Finally, there could be a common adaptation to a cool growing season. The Woodland Supplemental Material
FR is the only warm-growing-season radiation in southern Africa (although grassland grows in
summer, the summers are cooler due to the higher altitudes).
The Grassland FR spawned daughter radiations in all three other radiations. This is not sur-
prising as the Grassland system is intermediate ecologically between the other systems, sharing
environmental commonalities with each. The strictly alpine radiations have not seeded other radi-
ations, however, possibly because the alpine environment is too different to allow alpine-adapted
lineages to compete successfully elsewhere. A more likely argument is that these alpine radiations
are too young, and that there has not been enough opportunity or enough taxonomic diversity to
spawn daughter radiations.
The arid regions contributed the second largest number of lineages to other radiations. These
are largely derived from the initial Paleogene Desert FR, but several of the seeding events are recent
and are derived from the Miocene succulent karoo FR. This pattern is also found in animals, both
from the Paleogene (Pickford et al. 2014) and the Miocene (Pickford 2004) aridification events.
Thus, there is substantial between-radiation cross-fertilization. Sometimes this results in large
nested radiations (e.g., Disa in the Fynbos FR), but often the result is numerous small nested
radiations. The absence of such cross-fertilization might well result in FRs being much less species-
rich. The directionality of the flows (but not their volume) is related to the relative average ages of
the radiations. Older radiations donate more lineages than they receive, whereas the inverse is true
for younger radiations. The Woodland FR is the oldest (also consistent with the fossil record) and

Table 4 Southern African floristic radiations (FRs) that seeded daughter radiations on other continents, summarized from
Supplemental Table 4
Southern African source Northern
FR Australasia Eurasia Americas Hemisphere Global Total
Open habitats (fynbos, 4 0 0 1 2 7
desert, grassland)
Fynbos 3 0 0 0 2 5
Desert 0 1 0 0 2 3
Grassland 0 1 0 1 0 2
Woodland 0 0 0 0 0 0
Total 7 2 0 2 6 17
Supplemental Material has seeded three radiations, but has, itself, been seeded only once. By contrast, the Grassland FR
is the youngest and has received almost twice as many lineages as it has donated. The alpine FR
(which was not analyzed separately) most likely received numerous lineages and donated none. The
volume of the interchange among the radiations is more related to habitat similarity and possibly
the size of the floras: Most interchange is between the large cool-growing-season FRs (Desert,
Fynbos, Grassland), while the smaller warm-growing-season Woodland FR is relatively isolated.
Southern African Exports

The important role of intercontinental dispersal in building global biodiversity has long been
appreciated and has been the subject of considerable analysis (Crisp et al. 2009, Thorne 1973).
The southern African radiation has spawned daughter radiations on almost all other continents
(Table 4 and Supplemental Table 4), but the several FRs have contributed differentially to this
export. We suggest that the probability of lineage export depends on (a) the size of the southern
African radiation and, thus, its ecological amplitude; (b) the age of the radiation, which dictates
the time available for long-distance dispersal; and (c) the degree of habitat similarity.
We used the phylogenies compiled to explore nested radiations in southern Africa and the
literature to document several striking patterns in the export of southern African lineages. First,
there is no seeding of South American radiations. This may be due to the West Wind Drift (Muñoz
et al. 2004) that blows from South America to Africa. Second, radiations in North America reached
that continent via Europe (i.e., Crassulaceae, Scrophulariaceae). Third, most seeded radiations are
in Australasia (seven radiations in total), and they are all sourced from lineages that either form
part of the Fynbos FR (four radiations) or are shared between this FR and the two other open
habitat FRs (i.e., Grassland and Desert) (three radiations). Because the Fynbos FR associates with
strongly oligotrophic soils similar to those that are widespread in Australia, biome compatibility
(Crisp et al. 2009) has likely been influential in favoring lineage interchange between these areas.
The prevailing westerly winds in the southern oceans (Bergh & Linder 2009, Sanmartı́n et al.
2007) may also have favored dispersal from the Cape to Australasia. Fourth, desert radiations did
not seed radiations restricted to Australia; instead they tended to precipitate global or Northern
Hemisphere radiations. Finally, the Woodland FR, despite its great age, did not spawn daughter
radiations on other continents. This could be due to the much smaller diversity in the Woodland
FR or be a consequence of extensive extinction in the Woodland FR, thus removing evidence of
southern African sources of radiations on other continents. Evidence of global connectivity is thus
found from throughout the Cenozoic, and over all major clades of angiosperms, and suggests that
the southern African radiation contributed significantly to the global radiation of angiosperms.

DISCUSSION
A Southern African Scenario

Cape Fold
There is fossil evidence for the presence of present-day Fynbos (Restionaceae) and Woodland Mountains:
(Podocarpaceae, Araucariaceae, Chloranthaceae) clades in the southern African Paleogene. Based mountains at the
on molecular dating, we suggest that the flora of southern Africa was already differentiated into southern tip of Africa,
four ecologically separated FRs by the start of the Neogene: (a) a radiation of cool-adapted with two axes of folds
parallel to the
lineages on the uplands of the south–central African plateau (e.g., Hyacinthaceae, Orchidaceae, coastlines of the
Podocarpaceae); (b) radiation of a more tropical, woody flora on the eastern coastal plain (e.g., Atlantic and the Indian
Mimosoideae); (c) a radiation of edaphically specialized lineages on the oligotrophic soils of Oceans
the Cape Fold Mountains (e.g., Iridaceae, Proteaceae, Restionaceae); and (d ) radiation of an
more arid-adapted flora on the western escarpment and coastal plain, especially in Namibia
(e.g., Crassulaceae, Scrophulariaceae). The widespread Miocene records of woodland and forest
elements suggest that this vegetation was very widespread, with desert and fynbos elements
respectively restricted to the current Namibian coast and the sandstone outcrops of the Cape Fold
Mountains.
During the Miocene, the vast, cool central plateau may have been transformed by increasing
aridity and cooler temperatures from a temperate forest and/or woodland, first (mid-Miocene)
to a C3 grassland and finally (Pliocene) to a pyrophytic C4 grassland. The south- and westward
spread of this latter formation may have been limited both by the oligotrophic soils of the Cape
region and the predominantly winter-rainfall regime of the western escarpment and coastal plain.
Forest and woodland, under this scenario, were increasingly restricted to protected gullies and
the more mesic slopes on the eastern escarpment, and this restriction precipitated an attrition of
their species diversity.
The Late Miocene development of summer drought along the western margins of the sub-
continent (a Mediterranean-type climate) may have had two consequences. Along the central and
northern parts of this coast, the critically low rainfall led to the development of the hyperarid
conditions that characterize the modern Namib Desert, whereas somewhat moister conditions to
the south prompted the radiation of a succulent flora (Aizoaceae, Crassulaceae), which is also rich
in annuals (Scrophulariaceae). In the southern part of the coast, the summer drought contributed
to the ecological isolation of the fynbos flora on the oligotrophic Cape Fold sandstones.
The Pliocene uplift of the eastern escarpment strengthened the rain shadow to the west, thereby
exacerbating aridity along the West Coast. By raising the elevation of the already high Lesotho
plateau (the remnants of the Gondwanan surface), this led to the evolution of an alpine flora on the
Drakensberg. The Plio–Pleistocene climatic fluctuations likely stimulated an east–west oscillation
in the western limit of the summer rainfall (Chase & Meadows 2007). Elevated summer rainfall
in the southeastern Cape during the glacial phases may have facilitated the spread of C4 grasses
there, resulting in increased fire frequencies and a reduction in fynbos diversity relative to that in
the more protected southwest.
Why Is the Fynbos Floristic Radiation Richer than the Other

Three Floristic Radiations?
This scenario leads to several questions, the most prominent of which is: why are there such
dramatic differences in richness among the four FRs? Two of the FRs are globally exceptionally
species-rich (the Fynbos and Desert FRs), while the other two appear unremarkable (the Woodland
and Grassland FRs).

The much greater diversity of the Fynbos FR cannot be due to more time available because our
scenario suggests that both the Desert and Forest FRs are of comparable age to the Fynbos FR. The
Fynbos FR may have been less affected by climate fluctuations than the other radiations, possibly
on account of the oligotrophic soils with which it associates. The Cape Fold Mountains are built
of sandstones that weather to produce acutely nutrient-deficient acidic soils (Cramer et al. 2014),
and the floras supported by these soils are apparently more resilient to climate change than those
on less oligotrophic soils (Damschen et al. 2012). Furthermore, owing to the acute physiological
demands imposed by such soils (Cramer et al. 2014), they may be more resistant to invasion than
normal soils, and may consequently resist invasion by all but those lineages possessing the traits
required to exploit them. This may slow the rate at which Fynbos FR lineages are competitively
replaced by other lineages, even where the latter are better adapted to the local climate (Ackerly
et al. 2014, Verboom et al. 2014).
The Fynbos FR is also very species-rich compared with other regional Mediterranean-type
radiations, including the Australian Kwongan, which is similarly protected by its acutely oligo-
trophic soils. Possibly the greater richness in the Cape is due to its greater climatic heterogeneity
( Jiménez & Ricklefs 2014, Litsios et al. 2014), which has been implicated in the greater diversity
of Restionaceae in the Cape than in Australia (Linder et al. 2003). Furthermore, what is unusual
about the Cape is that although the landscape is steeply dissected, it is ancient. Whereas ancient
landscapes typically show a subdued or peneplained physiognomy, the Cape Fold Mountains,
situated on the southern coastal platform of Africa, are highly resistant to erosion, and so retain a
ruggedness that they have likely possessed throughout the Cenozoic (Scharf et al. 2013). A simi-
lar reasoning applies to the pediments of the mountains, which form an extensive duricrust that
erodes into steep river valleys and mesas at the slowest erosion rates known globally (Bierman
et al. 2014). The complex topography of the Cape region results in steep climatic gradients that
facilitate elevational isolation of populations during millions of years (Britton et al. 2014; Potts
et al. 2013a,b). This affords time not only for genetic differentiation and eventual speciation to
occur but also provides the refugia required to enable the products of divergence to persist.
The Drakensberg alpine FR is surprisingly species-poor. Although it consists of numerous small
radiations (in Poaceae, Scrophulariaceae, Hypoxidaceae, and Gentianaceae), none have built large
species flocks. The Drakensberg alpine ecosystem is presumably Pliocene in age, comparable
to the alpine ecosystems of the Andes (Gregory-Wodzicki 2000) and the New Zealand Alps
(Heenan & McGlone 2013). However, the Drakensberg shows no large radiations comparable
to the Andean Lupinus (Hughes & Eastwood 2006) or the New Zealand Veronica (Wagstaff et al.
2002). We suggest two reasons for this absence of major radiations: the relatively small area
of the Drakensberg above 1,800 m and the spatial cohesion of this alpine area, which forms a
continuous belt of high country along the eastern escarpment. This contrasts with the Andean
alpine zone, which is broken into numerous páramos, and the numerous islands of alpine habitat in
New Zealand. Thus, although fragmentation of the alpine zone may account for some speciation
(e.g., Bentley et al. 2014), the scale of such speciation is likely rather limited.
The rarity of Woodland radiations is equally striking. Woodland lineages have been recorded
throughout the Cenozoic in fossil sites in southern Africa, indicating that this is possibly the oldest
system in the area. The rarity of radiations applies not only to woody elements but also to the
associated epiphytic elements [but see Mystacidium (Orchidaceae)] and understory herbs [but see
Streptocarpus (Gesneriaceae)]. We suggest that this is due to a massive reduction in area, with
thicket and forest habitat transformed to grassland on the plateau, to succulent karoo along the
western escarpment and coastal plains, and to fynbos on the southern coastal plains. This is also
consistent with the extinctions evident from the fossil record.

How Important Are Complex Radiations?

The radiation of the southern African flora largely fits the predictions of a complex regional
radiation. The physical environment fits the predictions: the unusual geomorphology of two Peneplain: low-relief
peneplains separated by an escarpment, the high inland plateau, and the wedging between a warm plain in the final stages
and a cold ocean current resulted in a complex, stable environment in which change was local of fluvial erosion to a
defined level or nick
and gradual. Likewise, the four individual FRs also fit the predictions: with much exchange of
point
lineages, temporally staggered radiations, and much seeding of extracontinental radiations. Less
easy to accommodate in this model is the apparent decimation of the Woodland FR without an
obvious successor FR toward the end of the Miocene.
Several regional radiations may benefit from being viewed and analyzed as complex radiations
rather than as singular radiations. Typical examples could include the Australian radiation (Crisp
& Cook 2013), with, inter alia, Proteaceae, Mimosoideae, and Myrtaceae represented in all local
radiations, from the heathy Kwongan (Hopper & Gioia 2004) to the eastern rainforests. Similarly,
in the apparently disparate radiations in the northern Andes (Saerkinen et al. 2012), Bromeliaceae
radiated during the Miocene across all habitats in this region, starting from an initial radiation in
the ancient Venezuelan tepuis (Givnish et al. 2014, Silvestro et al. 2013).
The complex radiation model emphasizes local exchanges of lineages, and suggests that the
number of local radiations may be increased by the regional availability of lineages. This is com-
plementary to the intercontinental recruitment of lineages into radiations, which appears to be
particularly important in alpine radiations [e.g., Lupinus in the Andes (Hughes & Eastwood 2006)],
numerous radiations in the New Zealand Alps (Winkworth et al. 2002), and the tropic–alpine radi-
ations in central Africa (Gehrke & Linder 2009). Similarly, Galley & Linder (2006) demonstrated
that many of the lineages making up the Cape flora were recruited from Australia or Eurasia. The
complex radiation model highlights local, often between-biome, recruitment, which means that it
is easier to adapt than to disperse. As such, this is contrary to the biome-conservation assumption
that it is easier to disperse than it is to adapt (Crisp et al. 2009, Donoghue 2008).
Complex regional radiation increases the diversity of locally radiating lineages not only in terms
of species number but also in terms of ecological diversity. Greater diversity, in turn, enhances
the success of long-distance dispersal to other regions by providing a wider range of options for
overcoming obstacles to successful establishment. This may well explain why the southern African
flora has frequently functioned as a source area for the seeding of complex radiations elsewhere
on the planet [e.g., Gnaphalieae (Asteraceae), Scrophulariaceae, Crassulaceae, Amaryllidoideae
(Amaryllidaceae), Orchideae (Orchidaceae), Danthonioideae (Poaceae), Apioideae (Apiaceae)].
As exemplified by the southern African radiation, therefore, it seems likely that complex
radiations contribute significantly not only to local and regional diversity but also to global
biodiversity.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
ACKNOWLEDGMENTS
For tree topologies, we thank Antoine Nicolas (Apiaceae), Herve Sauquet (Proteaceae),
Jan Schnitzler (Protea), Bengt Oxelman (Scrophulariaceae), Sven Buerki and Felix Forest
(Hyacinthaceae), and Yanis Bouchenak-Khelladi (Mimosoideae).

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ES46CH18-Linder ARI 7 November 2015 10:57

H. Peter Linder1 and G. Anthony Verboom2

Annu. Rev. Ecol. Evol. Syst. 2015. 46:393–412 Keywords

394 Linder · Verboom

Complex radiations should generate a distinctive macroevolutionary signature, enabling them

SOUTHERN AFRICA AS AN EXAMPLE

www.annualreviews.org • Evolution of Regional Species Richness 395

396 Linder · Verboom

Table 1 Summary of the environmental history of southern Africa

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globally (Bierman et al. 2014). Much of the erosion was

398 Linder · Verboom

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Table 2 Major Cenozoic fossil sites in southern Africaa

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PREDICTED PATTERNS OF RADIATIONS

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Nested Southern African Patterns

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Number of crown radiations

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Southern African Exports

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A Southern African Scenario

Why Is the Fynbos Floristic Radiation Richer than the Other

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406 Linder · Verboom

How Important Are Complex Radiations?

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phylloideae as an example. Syst. Bot. 37:951–59

408 Linder · Verboom

Mol. Phylogenetics Evol. 43:60–74

www.annualreviews.org • Evolution of Regional Species Richness 409

410 Linder · Verboom

www.annualreviews.org • Evolution of Regional Species Richness 411

412 Linder · Verboom

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