Panbiogeography, its critics, and the case of the

CSIRO PUBLISHING
Australian Systematic Botany, 2014, 27, 241–256
http://dx.doi.org/10.1071/SB14027
Viewpoint
Panbiogeography, its critics, and the case of the ratite birds
Michael Heads
Buffalo Museum of Science, 1020 Humboldt Parkway, Buffalo, NY 14211-1293, USA.
Email: m.j.heads@gmail.com
Abstract. Panbiogeographic analysis is now used by many authors, but it has been criticised in recent reviews, with some
critics even suggesting that studies using the method should not be accepted for publication. The critics have argued that
panbiogeography is creationist, that it rejects dispersal, that its analyses are disingenuous, and that it deliberately ignores
or misrepresents key evidence. These claims are examined here, and are all shown to be without foundation. The
distributions of the molecular clades of ratites have not been mapped before, and they are considered here in some more
detail as a case study illustrating panbiogeographic methodology.
Received 24 August 2014, accepted 10 October 2014, published online 31 March 2015
Introduction
(1) ‘Panbiogeography is creationist’
Panbiogeographic methods for investigating distribution and
evolution are now used widely, especially in Latin America.
Recent publications include Moreira et al. (2011), MayaMartínez et al. (2011), Rosas et al. (2011), Pires and Marinoni
(2011), Ribeiro and Eterovic (2011), Climo and Mahlfeld (2011),
Grehan (2011), Arzamendia and Giraudo (2012), Mayén-Estrada
and Aguilar-Aguilar (2012), Velásquez et al. (2012), Ferretti
et al. (2012), Heads (2012a, 2012b, 2012c, 2014), CamposSoldini et al. (2013), Echeverry and Morrone (2013), Gallo
et al. (2013), Goldani (2013, 2014) and Quijano-Abril et al.
(2014).
Although the methods and applications have drawn positive
reviews (e.g. Nelson 2012; James 2013), several recent papers
have criticised the methodology. Waters et al. (2013a) wrote:
‘. . .to convey our concerns that some mainstream evolutionary
journals continue to publish papers that, in our view, present
misleading accounts of biological evolution. Specifically, we
argue that ‘panbiogeographic’ studies of spatiotemporal
biological history . . . are detrimental to the progress of
biogeography. . .’. The authors criticised the ‘editorial and
review processes [that] continue to allow this misleading
approach to be promulgated. . .’ (p. 494).
The present paper examines whether or not there is any
substance to the criticism. Waters et al. (2013a) cited the
classic case of ratite biogeography as an example illustrating
the problems with panbiogeographic methods, and so this
particular group is examined in some more detail.
In debates about evolutionary biology, authors often assert that
their opponents are creationists. For example, Nelson and
Platnick (1984) argued that modern systematics has moved
beyond Darwinism; Dawkins (1986, p. 284), seeing an attack
on Darwinism as an attack on evolution itself, responded that
Nelson and Platnick ‘have earned themselves a place of honour
in the fundamentalist, creationist literature’. (Other examples are
given by Livingstone 2013.)
McGlone (2005) wrote that panbiogeography supports
‘something close to special creation’, because it accepts a
mode of speciation (vicariance) that does not involve
dispersal. Waters (2005) suggested that including a discussion
of panbiogeography in a text book (Crisci et al. 2003) was ‘akin
to presenting creationism and evolution as two ‘equal’ scientific
disciplines. . .’. Waters did not describe how panbiogeography
resembles creationism, but O’Grady et al. (2012) did. They
argued that panbiogeographers are ‘like creationists’ as their
approach:
Criticisms of panbiogeographic analysis
Recent critics have proposed four main arguments, namely, that
(1) panbiogeography is creationist, that (2) it rejects dispersal,
that (3) its analyses are disingenuous and (4) that it ignores or
misrepresents key evidence (Holland 2012; O’Grady et al. 2012;
Waters et al. 2013a). These four claims are examined next.
Journal compilation CSIRO 2014
. . .is analogous to the wedge strategy proposed by
creationists and advocates of intelligent design. First, a
case is made that dogmatic thinking has overtaken good
science due to researchers viewing their data only with
a single lens, eliminating hypotheses because of
institutionalized biases within the field. Then, a ‘theory’
is presented as a reasonable alternative on equal footing
with the current dogma. [O’Grady et al. 2012, p. 703]
Yet this is the strategy used in many scientific studies; a
typical enquiry establishes that a standard model does not
account for observed phenomena and, on the basis of the
evidence, an alternative explanation is proposed.
Waters et al. (2013a) wrote ‘when panbiogeographic
hypotheses of ancient vicariance conflict with data from
geology, palaeontology and molecular genetics (as they almost
www.publish.csiro.au/journals/asb
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Australian Systematic Botany
inevitably do), panbiogeographers tend to dismiss these other
information sources as unreliable’. The authors did not cite any
actual data that do conflict (there are none), but the idea that
there is a conflict provides a basis for their conclusion: ‘this
attitude is akin to a young-earth creationist insisting that
the world was created in 4004 BC. . .’. The reason for this
heightened rhetoric is not because panbiogeographic results
conflict with the primary data, but because they challenge
the traditional interpretations of the Modern Synthesis, as
supported by Waters et al. (2013a).
Holland (2012) compared panbiogeography with ‘other
efforts aimed at undermining confidence in empirical science,
namely the creationist/intelligent design and climate change
denial movements. Similarities in approach include attempts
to cast doubt, exaggerate controversy and overplay scientific
uncertainty where convenient, in support of the agenda’. Thus,
any biologist who ‘casts doubt’ on orthodox theory is against
empirical science and resembles a creationist. This perspective
can be contrasted with the idea that doubt is a good thing in
science, as supported by authors such as Canetti (1962), who
wrote that ‘a scholar’s strength consists in concentrating all
doubt onto his special subject’. Rational scepticism does not
undermine confidence in empirical science, it is the basis of it
and the reason for it. Thus, the motto of the Royal Society is
‘Nullius in verba’, that is, ‘take nobody’s word for it’.
(2) ‘Panbiogeography does not accept that plants
and animals disperse’
Holland (2012) suggested that ‘panbiogeographers strongly
reject the significance of dispersal a priori, in any form. . .’
and that they ‘vehemently deny, a priori, any role of dispersal
in natural history’. Likewise, O’Grady et al. (2012) wrote that
panbiogeography involves ‘biased approaches that reject
dispersal a priori’ and Waters et al. (2013a) agreed, using the
same phrase verbatim. However, even young children know
that animals and plants disperse, and the suggestion that
panbiogeography rejects dispersal is simply not true; it is a
strawman created by the critics.
Waters et al. (2013a) wrote that ‘we have yet to see an
empirical panbiogeographic study that argues for anything
other than the primacy of some ancient vicariant process to
explain distributional data’ (p. 495). O’Grady et al. (2012)
proposed that ‘a central tenet of Heads’s (2012a) perspective
on biogeography is that most patterns observed can be explained
by the breakup or intercalary extinction of widespread
metapopulations’. These claims are not correct though, and
vicariance explains only allopatry, not distributional overlap. If
vicariance were the only process, every area on Earth would
have only one endemic clade. In fact, of course, many groups
have overlapping distributions, and in panbiogography, this
is attributed to dispersal (rather than sympatric speciation).
For example, the widespread overlap of primate clades by
range expansion (dispersal) in America, Africa and Asia, is
discussed at length in the book (Heads 2012a) that O’Grady
et al. (2012) and Waters et al. (2013a) both cited.
Although panbiogeography does not reject dispersal, it
does question its significance in establishing distribution in
particular cases. For example, Waters et al. (2013a) wrote that
M. Heads
‘panbiogeographers routinely scorn the role of long-distance
dispersal in assembling oceanic island biotas. . .’ (p. 495), but
inferring unlikely events of long-distance dispersal from distant
continents to a young island is unnecessary if former islands
existed in its vicinity.
Waters et al. (2013a) wrote as follows: ‘unfortunately,
this a priori rejection of long-distance dispersal [by
panbiogeography] . . . ignores abundant evidence supporting
this important process’ (p. 494). As an example of work
ignored by panbiogeography, they cited Ali and Huber’s
(2010) explanation for the presence of lemurs on Madagascar.
Yet panbiogeography has not ignored this study; it was critiqued
in a work that Waters et al. (2013a) cited (Heads 2012a, pp. 117,
118).
All (or almost all) individual organisms have dispersed to
their present location. In addition, many clades have expanded
their range by dispersal, and this accounts for overlapping
distributions. These ideas are more or less uncontroversial,
although Darwin (1859) extrapolated further and assumed that
all clades have attained their range by expanding outwards
from a ‘centre of origin’. Clements (1909, p. 145) noted that
Darwin’s assumption that species evolved at one spot ‘seems
to be little more than inheritance from the special creationists’,
and Gadow (1909, p. 326) made a similar observation.
Nevertheless, the Modern Synthesis adopted the centre-oforigin model. Mayr (1965) concluded as follows: ‘quite
obviously, except for a few extreme [local] endemics, every
species is a colonizer because it would not have the range it
has, if it had not spread there by range expansion, by
‘colonization’, from some original place of origin’. In a later
discussion of speciation, Mayr (1982) wrote that although
some textbooks showed ‘a widespread species cut in half by a
geographical barrier’, ‘more detailed studies . . . suggest a
different solution’, namely speciation by founder dispersal.
Stebbins (1966, fig. 5-1) agreed with Mayr and showed
allopatric differentiation developing solely by migration and
ecological differentiation; there was no mention of the
appearance of new geographic barriers. In other widely used
text books on speciation, Grant (1971, 1981, 1985) included
many maps of allopatry but, like Stebbins, did not mention
geographic change as a cause of allopatric speciation.
This assumption of a centre of origin and dispersal is
supported by many ecologists (for example, Levin 2000)
and palaeontologists (Eldredge et al. 2005); however, it is this
a priori acceptance of the assumption that panbiogeography
rejects. Following the early work in panbiogeography, the
importance of vicariance is now generally acknowledged
(in 1973 the term was cited 10 times, and in 2013 it was cited
1850 times; Google Scholar, accessed 20 July 2014).
(3) ‘Panbiogeography is disingenuous’
A panbiogeographic treatment of the Hawaiian Islands cited
former high islands in the Pacific that are now submerged, and
mapped the 2000-, 4000- and 5000-m isobaths of the central
Pacific (Heads 2012a, figs 7-1, 7-2). In response, Holland (2012)
wrote that ‘the figures appear to be a disingenuous and
misleading depiction aimed at advancing the vicariant agenda’.
O’Grady et al. (2012) agreed that the figures were ‘more than
Panbiogeography, its critics, and the case of the ratite birds
slightly disingenuous’, because sea level has not dropped by
more than ~100 m and so the submerged seamounts could not
have been emergent. Yet the authors overlooked the thousands
of metres of subsidence that the Pacific seafloor itself has
undergone through the Cenozoic (van der Pluijm and Marshak
2004, p. 404; Hillier and Watts 2005; Zhong et al. 2007, fig. 1).
As the seafloor has drifted away from the spreading ridge that
produced it, namely the East Pacific Rise, it has cooled (increasing
its density) over tens of millions of years, and it has subsided by
these large amounts. This has led to the submergence of most of
the earlier islands that had developed on it; the current high
islands are new ones. Some of the most obvious evidence for
subsidence is seen in the numerous atolls of the region. These are
constructed from coral reefs that have grown on former islands
as the seafloor and the islands subsided. In addition, the many
flat-topped seamounts (guyots) in the Pacific, for example, at the
north-western end of the Hawaiian–Emperor chain, are former
high islands that were eroded to sea level before being submerged
with the tectonic subsidence of the seafloor. Guyots also occur
north, south and west of the Hawaiian–Emperor chain (Etnoyer
et al. 2010; Heads 2012a; Gardner et al. 2013). All fresh lava on
Hawaii has been colonised by organisms from somewhere else,
but not necessarily from the nearest continent, thousands of
miles away.
In Heads (2012a), I listed several unjustified assumptions that
have been made about Hawaiian biogeography. The first was
the flawed reasoning that ‘the Hawaiian Islands have never been
connected to other land masses and so must have received all
their biota by long distance dispersal from the continents
(mainly Asia and America)’ (Heads 2012a, p. 314). Although
the first part of the sentence is correct, the second does not follow
from it if there were prior islands closer to Hawaii than the
continents. In their response to what I wrote, O’Grady et al.
(2012) commented that ‘one cited ‘assumption’ is that the
Hawaiian Islands have never been connected to other land
masses, despite all the data supporting these islands as a
young, volcanic hotspot archipelago’. This is disingenuous,
because I never suggested that the Hawaiian Islands have been
connected with other land masses.
(4) ‘Panbiogeography ignores or misrepresents
key evidence’
Waters et al. (2013a) suggested that panbiogeography
‘simply ignores the [past 25 years] of scientific progress
in evolutionary theory, molecular genetics, computational
biology and geology’ (p. 496). Yet, panbiogeogaphic studies
have discussed many papers on all these topics (more than 2000,
most published in the past decade, were referred to in Heads
2012a, 2014 alone). For example, with respect to geology,
panbiogeography has considered the biological significance
of guyots in the Musicians Seamounts north of Hawaii, the
boundary between the accreted terranes and the craton in
northern South America, the Central African Rift System (not
the Great Rift), the terranes of Borneo, New Caledonia and
New Zealand, uplift and subsidence in Fiji, strike-slip
displacement on major faults in New Zealand and New
Caledonia, and many other features, none of which had
previously been cited by biogeographers.
Australian Systematic Botany
243
Waters et al. (2013a) also wrote that ‘panbiogeographers
have proposed scenarios that seemingly dismiss all other
data regarding the history of life on Earth. . .’ (p. 495).
Panbiogeographic work has rejected certain interpretations and
hypotheses, but not data. The method relies on a wide range of
recent data from biogeography, phylogenetics, palaeontology
and tectonics. The critics disagree, not because we failed to
refer to the molecular and geological data, but because we
gave a novel interpretation of the data that they had not
considered. The strange assertion that ‘The panbiogeographic
approach usually ignores long-distance dispersal’ (Waters et al.
2013a, p. 494) again overlooks the detailed critiques of all
aspects of the topic made by panbiogeographers over the past
50 years.
Biogeography and fossils: the problem of the priors
Holland (2012) argued that panbiogeography discounts the
use of fossil ages to estimate lineage ages; however, this is not
correct. Whenever they are available, fossils and their ages
are incorporated in panbiogeographic analyses of particular
groups (e.g. Heads 2012a). What the method does reject is the
idea that maximum possible clade ages can be ascertained by a
literal reading of the fossil record. Instead, the age of the
oldest known fossil of a group is taken to represent a
minimum age for its clade. As Smith (2007, p. 231) wrote,
‘the fossil record provides direct evidence but it cannot be
taken at face value’.
The same principle applies to fossil-calibrated clock
studies. Waters et al. (2013a) wrote that ‘practitioners of the
panbiogeographic approach routinely deny the utility of
molecular-clock dating, presumably because molecular date
estimates are usually much younger than those expected under
vicariance’ (p. 496). Panbiogeography rejects the treatment of
fossil-calibrated molecular clock dates as maximum (absolute)
clade ages, and instead it interprets them as minimum ages.
The technical problems involved in treating fossil-calibrated
clade ages as maximum ages are explained in more detail in a
paper on Bayesian dating (Heads 2012b). (Although this was
published 3 months before Waters et al. (2013a) submitted
their paper, it was overlooked in their critique). The key
question is: just how much older than its oldest fossil can a
clade be? In Bayesian studies, authors stipulate as ‘priors’, before
any analysis, that the maximum age of a group can be no more
than an arbitrary number of years older than the oldest fossil. The
authors are free to choose any number, but in practice, the number
chosen is usually very small, reflecting the traditional, illogical
idea that a group is only a little older than its oldest fossil. The
priors mean that young ages are calculated for the clades. This,
in turn, means that vicariance can be ruled out and the traditional
model of chance dispersal supported. Although the method is very
popular, the ‘problem of the priors’ is now being acknowledged
by a growing number of authors (see papers cited in Heads
2012b). For example, a recent discussion of the problem
concluded that sporadic preservation in the fossil record ‘may
be effectively impossible to model’ and that priors ‘should . . . be
regarded as highly arbitrary’; their value ‘is something we simply
cannot know’ (Pirie and Doyle 2012, pp. 108, 109).
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M. Heads
Central Pacific biogeography
According to Holland (2012), panbiogeography ‘suggests
that arcs of once-emergent ancient seamounts between, say, the
Hawaiian and Marquesan islands played a role, by harboring the
lineages we see today . . . over tens of millions of years. But
again this would require numerous departures from what is
understood and accepted by geophysicists’. In fact, this model
would not involve any departures from standard geology,
because it is well known that the many atolls and seamounts
between French Polynesia and Hawaii (the Line Islands) are
former high islands, produced during multiple phases of
volcanism (but not, despite Holland’s (2012) suggestion, as
arcs). Earlier dispersalists recognised this; Zimmerman (1948,
p. 127) wrote that ‘many of the peculiar endemic groups of the
Hawaiian and south-eastern Polynesian islands owe their
existence, if not their very origin, to ancient high islands of the
one-time splendid archipelagos now marked by clusters of coral
reefs [or submerged seamounts]. . . Atolls have been overlooked,
generally’. Sixty years later, the atolls and seamounts that
surround the Hawaiian Islands are still neglected by dispersal
theorists. Where they are acknowledged, the former islands
that they represent are regarded merely as stepping stones that
may have facilitated dispersal from the Pacific margins to the
Hawaiian Islands (e.g. Mayr 1982, p. 453). However, former
islands may have had a more fundamental role than this, because
the different generations of islands could have allowed lineages
to persist in the region since the Jurassic, at least.
Waters et al. (2013a) suggested that instead of accepting
long-distance dispersal, panbiogeography invokes ‘continental
land bridges and island arcs of little or no geological
credibility (see critique by O’Grady et al. 2012)’ (p. 495). This
is a serious charge, but neither Waters et al. (2013a) nor
O’Grady et al. 2012 provided a single actual example; this
is because there is none. Again, the authors are attacking
strawman arguments that panbiogeography has never
advocated, to avoid confronting real issues such as the
significance of the seamounts, the relevance of slab rollback
for vicariance, the problem of the dating priors (see above), and
many others.
O’Grady et al. (2012) suggested that ‘a plethora of data,
such as the well understood geological processes involved in
the formation of the Hawaiian Archipelago . . . are ignored
[by Heads 2012a]’. In fact, Hawaiian geology is controversial.
Instead of ignoring the problems though, I cited many new
studies on the topic that have not been mentioned before
in biological work, and I discussed their implications. The
underlying causes of Hawaiian volcanism are a topic of
intense current debate. For example, is the proposed hotspot
beneath Hawaii hotter than the surrounding mantle? Earlier
work (cited in Heads 2012a) suggested that it is not, and a
subsequent study by Presnall and Gudfinnsson (2011) also
concluded that ‘Hawaii is not a hot plume. Instead, it shows
magmas characteristic of normal mature-ocean thermal
conditions in the low-velocity zone. We find no evidence of
anomalously high temperatures of magma extraction and no
role for hot mantle plumes. . .’. Presnall and Gudfinnsson
(2011) developed a model for the Hawaiian volcanism that
involves fracturing of the seismic lithosphere, not mantle
plumes. Hamilton (2011) concluded that ‘all published
tomographic models of purported deep plumes are severely
According to Holland (2012), panbiogeography accepts that
‘there were emergent Pacific land masses, some of which
connected the far-flung island archipelagos and continents
surrounding the Pacific basin. . .’. This is not correct; for the
central Pacific, panbiogeography accepts a complex history of
volcanic islands and oceanic plateaus that have undergone
subsidence, uplift, rifting, horizontal translation and accretion.
It does not accept land masses connecting far-flung
archipelagos. Panbiogeography adopts a metapopulation
model, in which a widespread ancestor survives in situ, which
may be a large region of the central Pacific, by colonising
individually ephemeral islands as these become available.
Colonisation is by whole populations using normal means of
dispersal, not by individuals undergoing rare founder events
that lead to speciation. Thus, the same metapopulation model
that applies to groups occupying habitat ‘islands’ on continents
also applies to populations on real islands in an ocean. In
contrast, dispersal theorists reject a metapopulation model and
local dispersal among islands, but at the same time accept
founder dispersal from continents thousands of kilometres
away.
Many authors have suggested that ‘vicariance cannot
explain endemic species on oceanic islands. . .’ (Coyne and
Orr 2004, p. 124), but this is not correct. Migration of
subduction zones and their associated island arcs away from a
continent or from other islands (by slab rollback) is one
important mechanism, rifting of active island arcs is another.
The Solomon Islands–Vanuatu–Fiji–Tonga arc has undergone
both processes, migrating away from the Gondwana mainland
in the Cretaceous, and then itself being rifted apart between
Vanuatu and Fiji (Heads 2014).
In a discussion of the central Pacific, Holland (2012)
criticised the idea that submerged seafloor structures, ‘e.g.,
Heads’ [2012a] so-called ‘Mid-Pacific Mountains’ ’, were
formerly emergent. Holland wrote that ‘this extraordinary idea
was proposed in various iterations in the 18th and 19th centuries’
and, even though the idea ‘sounds peculiar today’, the mistake
can be attributed to the primitive technology of the time
(‘wooden sailing ships, sextants and sounding lines’). Holland
suggested that geologists using modern techniques (such as
‘K–Ar radiocarbon dating’ [sic]) have rejected the ‘midPacific plate hypothesis’, and ‘so the panbiogeographers
intentionally . . . ignore or misinterpret many important
advances in natural science. . .’.
Despite Holland’s (2012) claims, no-one has rejected the
‘mid-Pacific plate hypothesis’; it is common knowledge that
many Pacific seamounts are former islands; and the term ‘MidPacific Mountains’ is not my own; it is the standard name for a
large, well known, submarine mountain range. This range forms
a system together with the atolls and seamounts of the Line
Islands, and both features are known to include many former
high islands (Firth 1993; Natland and Winterer 2005). Geological
studies continue to find good evidence for former islands in
the region, for example, on the Necker Ridge west of Hawaii
(Gardner et al. 2013). These structures have been neglected
by the modern dispersalists; however, they are discussed in
panbiogeographic work (Heads 2012a).
Panbiogeography, its critics, and the case of the ratite birds
flawed. . . I discuss here only Hawaii, which provides the type
example for rationalization of a ‘plume track’ while disregarding
both observed tectonic controls of magmatism and failure of
geophysical predictions in plume speculations. . .’. Another
study of Hawaii proposed that ‘lithospheric architecture and
stress control the locations of volcanoes, not localised thermal
anomalies or deep mantle plumes’ (Anderson 2011). Foulger
(2012) concluded that the Hawaiian melting anomaly
(‘hotspot’) is neither hot nor a spot.
According to Holland (2012, p. 317):
Heads [2012a] argues further, attempting to cast doubt on
established geological principles, that the Pacific hot spot
position is not well characterized, that mantle plumes may
not exist, that the Hawaiian Islands may have once been
joined with other land masses, and ‘In fact the whole subject
of intraplate volcanism is currently being debated among
geologists’. I wonder which geologists?
There is no need to wonder though, because the debate
was fully referenced in the book that Holland cited (Heads
2012a). For example, the cited studies include two large
volumes that the Geological Society of America has devoted
to the topic (Foulger et al. 2005; Foulger and Jurdy 2007).
A recent critique of mantle-plume theory has been published
by Anderson (2013). Anderson is a leading geophysicist
(he is a recipient of the highest scientific honour of the US
government, the National Medal of Science), and although the
idea that I am the one ‘attempting to cast doubt on established
geological principles’ suits Holland’s (2012) story, it is supported
only by his deliberate ignorance of the geological literature that
I cited.
For the Hawaiian Islands, O’Grady et al. (2012) suggested
that ‘our well supported understanding of the geologic
processes underlying island formation precludes the
panbiogeographic persistence of metapopulations in any real
sense’. They based this criticism entirely on the idea that in
the Hawaiian Islands, ‘there have been times during the past
60 million years where few or no islands existed’. Yet this idea
overlooks a serious problem with the calculations it was based
on; namely, the method that was used underestimates the
heights of present volcanoes, and so it probably also
underestimates the heights of past islands (Heads 2012a, p.
319). Because of this, Waters (2007) was justified in
suggesting that Hawaiian Drosophila and also some elements
of the Galapagos biota are ‘relatively ancient, dating back to
historical (now ‘extinct’) islands’. O’Grady et al. (2012)
described the suggestion that a metapopulation could persist
indefinitely around an island-generating structure as a
‘fantastical conjecture’, but it has been accepted for the
Hawaiian Islands by many authors, including dispersalists
(Waters 2007) and geologists (Menard 1986), not just
panbiogeographers.
Holland (2012) wrote that ‘regarding the islands of Maui
and Hawaii, and against all geophysical evidence [none was
cited], Heads [2012a] states that ‘there may have been land
between the two islands’ (p. 357)’. This ignores the excellent
geological evidence that I cited for subsidence between the two
islands (now 50 km apart) caused by volcanic loading:
Australian Systematic Botany
245
Price and Elliott-Fisk (2004, fig. 5) plotted one of the
breaks-in-slope (their ‘H terrace’) for 125 km from
Molokai, where it is about 500 m deep, to east of Maui,
where it is over 2000 m deep. This means that the originally
horizontal feature has tilted as it subsided; the tilt has
resulted from higher rates of subsidence closer to the
current zone of volcanic loading, the volcanoes on Hawaii.
The profile of the H terrace, as far as it was mapped, shows
direct evidence for at least ~1500 m of subsidence and as
the sea between Maui and Hawaii is currently only between
1500 and 2000 m deep there may have been land between
the two islands [Heads 2012a, p. 357].
Whether Maui and Hawaii were actually joined or not is
unknown and unimportant; the point is that the sea gap
between them has increased over time with continued
subsidence, and this provides a possible mechanism for
vicariance in shallow-water and terrestrial groups. Organisms
that could disperse, say, 3 km across open ocean, could have
maintained an original metapopulation in Maui and Hawaii,
but they may not be able to disperse 50 km, and so, with
continuing subsidence, they could have diverged.
Chatham Islands biogeography
Elsewhere in the Pacific, the Chatham Islands of New Zealand
have a distinctive biota that includes many endemics.
Panbiogeographic work has argued, in agreement with
molecular-clock dates, that at least some of the endemics
predate the current islands (Heads 2011). Waters et al. (2013a)
wrote that ‘geological and palaeontological analyses . . . clearly
show that the islands themselves were completely submerged
until less than 10 Ma’ (p. 495). In fact, geologists have agreed
that islands existed in the area currently occupied by the
Chathams before 10 Ma, but that there were no emergent
islands from 6 until 3 Ma (Campbell 2008; Landis et al. 2008;
Campbell et al. 2008, 2009). Nevertheless, on the basis of older
clock dates for various plants endemic to the Chatham Islands,
Heenan et al. (2010) suggested that islands also existed in the
region between 6 and 3 Ma.
In addition to the islands that geologists have accepted in
the Chathams archipelago before 10 Ma, and the islands that
Heenan et al. (2010) proposed there between 6 and 3 Ma, there
is now excellent evidence for many, now-submerged seamounts
(former islands) around the Chatham Islands and the Chatham
Rise, lying between the islands and the New Zealand mainland
(Rowden et al. 2005). Multibeam surveys of seamounts around
part of the Chatham Rise have showed that the largest volcanic
cones are ~2000 m in diameter and that most of the cones have
flat tops (Collins et al. 2011), indicating erosion to sea level
before subsidence. Waters et al. (2013a) argued that: ‘. . .multiple
independent lines of evidence clearly indicate that the modern
Chatham Islands biota was established by trans-oceanic
dispersal [from the mainland]’ (p. 496), but they overlooked
the seamounts.
Biogeography and orogeny
Panbiogeographic work has indicated that present distributions
developed on past landscapes, not on present ones. Although
the former landscapes no longer exist, they can be inferred from
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Australian Systematic Botany
M. Heads
indirect evidence. Waters et al. (2013a) accepted that: ‘. . .the
geological record retains little or no preserved evidence of
topographic features in 200 million year old orogens’ (p. 496),
but, by definition, any orogen, whatever its age, constitutes
evidence for topographic features, namely mountains.
Waters et al. (2013a) argued that although ‘. . .there remains
abundant visible evidence of topographic barriers in young
[<5 Ma] mountain belts . . . panbiogeographers apparently
ignore the latter events’ (p. 496). Instead, panbiogeographers
‘routinely attribute such biological radiations to ancient
(>20 Ma) geological processes (e.g. Heads 1998; Heads and
Craw 2004; Heads 2012b, figs 5, 6), but without the
quantitative evidence needed to discount younger processes.’
The spatial evidence for rejecting particular features as
causative is straightforward. The New Zealand clades mapped
in the figures cited (Heads 2012b, fig. 5 showing skinks, and
fig. 6 showing harvestmen) have their main distributional
breaks at the Alpine fault, not at the main divide formed by
the uplift of the young mountains. In addition, the distributions
of the two groups each include marked dextral (right-lateral)
disjunctions. This means that the breaks cannot be explained by
later Neogene uplift without additional, ad hoc hypotheses.
Instead, they are consistent with an origin by earlier Neogene
strike-slip (horizontal) displacement along the Alpine fault.
Despite the claims of Waters et al. (2013a), panbiogeography
is not ‘fixated on ancient earth history’ (p. 494), because it also
considers the effects of Neogene Earth history. Apart from
proposing Neogene strike-slip displacement of communities in
New Zealand, panbiogeographic studies have concluded that
Neogene orogenic uplift has raised populations in New Zealand,
New Guinea, the Andes and elsewhere, and this has been
accepted by subsequent authors (for example, Ribas et al. 2007,
writing on Andean parrots). Nevertheless, many geographic
distributions do not coincide with young mountain belts.
Instead, clades in groups such as the New Zealand skinks and
harvestmen, cited above, show spatial coincidence with other
tectonic features, such as the Alpine fault (Heads and Craw
2004). This can also be seen in ratite birds, as the primary breaks
in clades of both kiwis and moas coincide with the Alpine fault,
not the main divide. This is discussed in the next section.
Ratite birds and plate tectonics
The ratites are the sister-group of all other extant birds, and
include the largest living birds (ostriches). They also include
the elephant birds (Aepyornithidae) of Madagascar, which are
largest of all known birds, living and fossil. The Aepyornithidae,
along with the moas (Dinornithidae) of New Zealand, went
extinct in historical times. All known ratites are flightless,
except the tinamous and the fossil group Lithornithidae.
Although they were named as a group, Ratitae Merrem, in
1813, the original delimitation of the group has now changed, to
include tinamous, and many authors refer to the new grouping
as Palaeognathae Pycraft 1900 (Phillips et al., 2010; Waters
et al. 2013a). Nevertheless, there is no need to change the
name of a group just because its delimitation changes. The
name Ratitae, or ratites, is much older and much more widely
known than Palaeognathae, and so it is used here.
The distribution of the ratites has intrigued biogeographers
for many years. Most of the patterns seen in the group, including
major trans-oceanic disjunctions, are also well known in other
animals and in plants, and so ratites have become a standard test
case for biogeographic theory.
Waters et al. (2013a) illustrated the methods of
panbiogeography using the example of the ratites. The authors
showed that the panbiogeographic analysis of the group given
in Craw et al. (1999), based on morphology, is inconsistent
with aspects of the latest phylogenies (Smith et al. 2013; cf.
Mitchell et al. 2014a). This is not surprising, because there
has been a molecular revolution in systematics over the past
15 years. The actual distributions of the molecular clades of
ratites are more interesting, and, because they have not been
mapped before, they are examined here briefly as a case study
showing how panbiogeographic methodology works.
Molecular phylogeny and distribution of the extant
and subfossil ratite clades
The extant and subfossil ratites comprise four main clades,
with the molecular phylogeny (Mitchell et al. 2014a) and
distributions (del Hoyo et al. 1992) shown in Figs 1 and 2.
Fossil ratites
As indicated above in the section ‘Biogeography and fossils’
section, it is sometimes suggested that panbiogeography ignores
the fossil record. This is not correct; any fossils that are known
are incorporated into dating and spatial analyses (for example, see
Heads 2012a, on primates). The advocates of dispersal theory
dispute this, not because panbiogeography ignores fossils, but
because it interprets them in a new way. It uses fossils to provide
Struthionidae (ostriches): Africa and (fossil) Eurasia
Rheidae (rheas): South America south of the Amazon
Aepyornithidae (elephant birds) + Apterygidae (kiwis);
Casuariidae (cassowaries) + Dromaiidae (emus): trans-Indian Ocean
Dinornithidae (moas) + Tinamidae (tinamous): trans-Pacific Ocean
Fig. 1. Molecular phylogeny of the extant and subfossil ratites (Mitchell et al. 2014a).
Panbiogeography, its critics, and the case of the ratite birds
x
x x
x
Australian Systematic Botany
x
x
x
x
x
x
Lithornithidae †
x
247
x
Tinamidae
Casuariidae
Struthionidae
Aepyornithidae †
Dromaiidae
Dinornithidae
1
Ratites 1 (2 (3 + 4))
†
2
4
3
Apterygidae
Rheidae
x
Fig. 2. Distribution of the ratites (phylogeny from Mitchell et al. 2014a, distributions from del Hoyo et al. 1992).
Fossil localities as X symbols. Putative ratite fossils from Seymour Island, northern Antarctic Peninsula, are indicated with
an arrow. Two localised fossil groups, Palaeotididae of Germany and Remiornithidae of France, are not shown. The
fossil record of Casuariidae from either Wellington Valley (New South Wales) or the Darling Downs (Queensland)
is also not shown.
minimum ages for clades, not maximum ages, and does not
assume that the oldest fossil represents a centre of origin.
In practice, many fossils, especially older ones, are very
difficult to identify and place on phylogenies, because they do
not include many critical morphological features (such as soft
parts) or any DNA. In many groups, a great deal of anagenetic
evolution, as well as cladogenesis, has occurred over time, and
fossils of a lineage from the Cretaceous, say, may be quite
different from the modern representatives. In ratites, the
affinities of many putative fossil members are controversial.
Overall, the fossil record of ratites is very poor. For
example, elephant birds have no pre-Pleistocene fossil record.
Kiwis (Worthy et al. 2013), moas (Tennyson et al. 2010),
ostriches (Mayr 2009) and tinamous (Mayr 2009) have no
fossils older than Miocene, and the oldest fossils of the
emu–cassowary lineage are Oligocene (Worthy et al. 2014).
The oldest rhea fossils are Paleocene (Feduccia 1996). (Note
that the sequence of appearance of the families in the fossil
record does not follow the phylogenetic sequence.)
In addition to the extant clades, ratites include three fossil
families. Lithornithidae are known from North America and
Europe (Paleocene to Eocene; Fig. 2), but the family’s exact
composition, whether or not it is monophyletic, and its position
in ratite phylogeny, are all unresolved (Mayr 2005). The
affinities of two fossil groups of ratites, the Palaeotididae of
Germany and the Remiornithidae of France, are also obscure
(Mayr 2009). Their distributions are local and are not shown
in Fig. 2.
Eleutherornis (Eleutherodactylidae) of Switzerland has
been regarded as a ratite, but there is no compelling evidence
for this identification (Mayr 2009). Eremopezus (including
Stromeria) is represented by Eocene fossils from Egypt and
was identified as Aepyornithdae (for example, Feduccia 1996),
but it is now placed in its own family, Eremopezidae, and its
status as a member of ratites has been questioned (Rasmussen
et al. 2001).
Some fossil eggshells not associated with bones have been
attributed to ratites, but their identification is ambiguous, and
ratite-like eggshells are also found in some extant, non-ratite
birds (Mayr 2011). Likewise, ‘aepyornithid-type’ eggshells are
widespread as fossils in Africa and Asia, but the similarities
with Aepyornithidae are likely to represent characters that are
plesiomorphic in ratites (Bibi et al. 2006).
No fossil ratites are known from mainland Antarctica.
There is putative ratite material from Seymour Island off the
Antarctic Peninsula, but nothing more can be said about its
affinities and even its identification as a ratite needs to be
verified (Mayr 2009). Ratites, living and fossil, are widespread
globally, and it would not be surprising if fossils were found in
India, Sri Lanka, South-east Asia or Antarctica.
Feduccia (1996, p. 285) argued that the northern
hemisphere fossil ratites ‘almost certainly evolved there
long after the breakup of Gondwanaland’, but this assumes,
illogically, that fossil dates give maximum rather than
minimum clade ages. The northern fossil forms have been
described as ‘ancestral ratites’ (Chatterjee 1997, p. 263), but
there is no evidence that the fossil families were ancestral to the
extant ones.
Distribution of the ratite clades
All the distribution patterns in the ratites could be the result of
chance dispersal events, that is, events that only occurred once in
the history of the lineage and were unrelated to any other
biological or physical factors. An alternative is a vicariance
model, beginning with a widespread ancestor.
The main feature of the distribution pattern of ratites
(Fig. 2) is its simplicity. Although the group is widespread
globally, the four main clades (and the Lithornithidae) are
allopatric everywhere except New Zealand and South America
south of the Amazon. This has not been mentioned by
previous authors, but it is consistent with an origin of the
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Australian Systematic Botany
clades by simple vicariance, followed by dispersal and local
overlap within New Zealand and South America. Allopatry as
a general pattern has been explained either by founder
dispersal or by vicariance. Allopatry by founder dispersal is
sometimes accounted for by a ‘founder takes all’ model, with
the colonising clade preventing any subsequent invasion by
competition (Waters et al. 2013b). In the ratites, this is
contradicted by the overlap of clades in New Zealand and
South America.
A panbiogeographic approach asks the following general
question: can a coherent synthesis of a group be constructed in
which the phylogenetic and distributional breaks (nodes) in the
group are correlated spatially with tectonic events in the same
region as the breaks? The phylogenetic and geological breaks
must appear in the same chronological sequence, and the clades
must be no younger than their oldest fossils or fossil-calibrated
clock dates.
The first node in the ratite phylogeny separates ostriches
(notably absent from Madagascar) from the rest. The break
corresponds with the Mozambique Channel, formed at ~160
Ma in the late Jurassic. Other parts of the break occur between
China (where there are ostrich fossils) and New Guinea (with
cassowaries).
The next node separates rheas and Clades 3–5. The
extensive overlap of rheas with tinamous obscures the site of
the original break; however, whereas rheas do not occur on the
western coast of South America, tinamous do, namely along
the coast of central Chile at 29–41S (The IUCN Red List
of Threatened Species, search ‘Tinamidae’ at www.iucnredlist.
org, accessed 23 November 2014). This region has many
biogeographic links with Australasia, for example, in
marsupials (Heads 2014, pp. 95, 96). Thus, the original break
is likely to have been located between rheas in south-eastern
South America and its sister in the west, with tinamous
subsequently expanding their range eastward.
The break between rheas in the east and, for example,
tinamous in the west corresponds spatially with a volcanic
mega-event, the third, and last pulse of Chon Aike volcanism
(138–157 Ma, latest Jurassic–earliest Cretaceous). This
occurred along the line of the future Andean cordillera. The
Chon Aike volcanic province extends from central Argentina
to Tierra del Fuego and West Antarctica, and is one of the
largest rhyolitic provinces in the world (Rapela et al. 2005).
The volcanism was a precursor of breakup in this part of
Gondwana.
Trans-Indian Ocean v. trans-Pacific Ocean allopatry
The differentiation of the ostriches and rheas leaves a diverse,
widespread Indo-Pacific group, comprising Clades 3 and 4, that
is examined here in some more detail. It comprises a transIndian Ocean group (Clade 3) and its sister, a trans-Pacific
group (Clade 4). A vicariance model for these two clades
predicts that other groups will have similar distributions, and
examples of these include the following:
In the conifer family Podocarpaceae, the trans-Indian
Ocean clade Afrocarpus + Nageia is sister to the transPacific Retrophyllum [Heads 2014, fig. 3.20, including
living and fossil records].
M. Heads
In angiosperms, the trans-Indian Ocean Salvadoraceae is
sister to the trans-Pacific pair Bataceae + Koeberlinaceae
[Heads 2014, fig. 3.19].
In the butterfly tribe Troidini (including the largest of all
butterflies, in New Guinea), the trans-Indian Ocean clade
Pharmacophagus + Cressida is sister to the trans-Pacific
clade Trigonoptera [Heads 2014, fig. 3.22].
A vicariance history also predicts that the same transIndian v. trans-Pacific pattern will also occur in groups with
different ecology, such as shallow-water marine groups. This
can be confirmed, because the mangrove genus Rhizophora, for
example, comprises a trans-Indian group (R. stylosa and
relatives) and its sister, a trans-Pacific clade (R. samoensis
and relatives) (Lo et al. 2014). Lo et al. (2014) wrote that their
‘comprehensive biogeographic study’ ‘revealed’ both transPacific and trans-Indian Ocean dispersal events; however, they
did not mention the allopatry of the two main clades, or the
possibility that the allopatry evolved by simple vicariance.
In New Zealand, Cooper et al. (1992) found that kiwis
(in the trans-Indian clade) and moas (in the trans-Pacific clade)
are not sister groups, and therefore, argued that ‘New Zealand
was probably colonized twice by ancestors of ratite birds’
(Cooper et al. 1992). Feduccia (1996, p. 278) described this as
an ‘inescapable conclusion’, but this is true only if a particular
model of ratite evolution, namely, a centre of origin model, is
assumed. As indicated, the allopatric distributions of the
known ratites are instead consistent with vicariance of a
worldwide ancestor. The ancestral Indo-Pacific clade divided
into kiwis and relatives around the Indian Ocean, and moas
and relatives around the Pacific, with the boundary running
through New Zealand. The Indian and Pacific clades
themselves then broke down into their modern subclades, the
families. In this model, neither moas nor kiwis colonised New
Zealand; they both evolved there.
India Ocean–Pacific Ocean allopatry explained
by prebreakup magmatism and orogeny
In their study of ratites, Phillips et al. (2010) examined the
biogeography of the group by estimating clade ages with
fossil-calibrated clock dates. They ruled out the presence of
the birds in Gondwana and a vicariance history for the group,
and instead suggested a dispersal model. Yet this idea depends
on the treatment of fossil-based clade ages, namely minimum
ages, as maximum ages (Heads 2012b).
Mitchell et al. (2014a) concluded instead that ‘molecular
dating provides limited power for testing hypotheses about
ratite biogeography. . .’, and this is accepted here. Instead of
focussing on estimated clade ages, Mitchell et al. (2014a)
concentrated on the branching sequence of the phylogeny. As
they observed, this is incongruent with the breakup sequence
of Gondwana, as seen in the break between the Indian Ocean
and Pacific clades. They noted, correctly, that the incongruence
eliminates a simple vicariance process caused by Gondwana
breakup. But they assumed, incorrectly, that this rules out any
vicariance model, and so they accepted that the pattern must
have resulted from chance founder dispersal. This argument
involves two mistakes, the assumption that the breakup
Panbiogeography, its critics, and the case of the ratite birds
Australian Systematic Botany
process begins (rather than ends) with seafloor spreading,
and the idea that the breakup of Pangaea and Gondwana
represents the only possible mode of global vicariance. The
first step in the differentiation of the modern ratites, namely,
the separation of the ostrich lineage from the rest, can be
explained by initial Gondwana breakup (including between
mainland Africa and Madagascar at the Mozambique
Channel), but the breakup of the Indo-Pacific clade cannot.
Instead, it is attributed here to tectonic events that took place
in the lead up to seafloor spreading.
One possible mechanism for the Indian-Pacific break is
the development of the Australides. This was a mountain belt
located along the margin of southern Gondwana in areas that
became southern and western South America, western
Antarctica and eastern Australasia (Fig. 3). In New Zealand,
the last phases of the Australides uplift are recognised as the
Rangitata orogeny. The formation of the Gondwanide belt
and its successor, the Australides belt, was caused by
subduction and terrane accretion along the Gondwana margin
from Neoproterozoic (pre-Cambrian) to late Mesozoic time
(Vaughan et al. 2005). The Australides region is well known
to biogeographers as a major centre of endemism that does
not involve the core cratonic areas of Gondwana including
eastern South America, Africa India and Western Australia
(Gibbs 2006). Thus Australides (‘Pacific’) distributions are
distinct from ‘core Gondwana’ patterns that straddle the Indian
and Atlantic Ocean basins.
Development of the Australides continued through the
Mesozoic until backarc spreading began behind the arc (on the
continent side) and led to rifting, backarc basin formation and
Gondwana breakup. Whereas the Australides developed as a
gently curved feature, convex towards the ocean (Fig. 3),
249
during Gondwana breakup, the orogen was recurved into a
semi-circular, concave structure that now surrounds the South
Pacific.
Along with the subduction, accretion and uplift, the
Australides belt was also the site of large-scale magmatism.
The Whitsunday volcanic province off eastern Queensland
(132–95 Ma) has equivalent rocks in New Zealand (Median
batholith; with the last phase, in Fiordland and Nelson, taking
place at 130–105 Ma) and in Marie Byrd Land, West Antarctica.
This belt as a whole, mainly composed of Early Cretaceous
granite and rhyolite, forms the Earth’s largest silicic igneous
province (Fig. 4, from Heads 2014). Its emplacement, over
~30 million years, was one of the last events in the history of
the Australides.
The Australides belt developed over a long period of time
and in multiple active phases, with the active zone of
subduction, accretion, magmatism and orogeny progressing
steadily oceanward. The episodes of tectonism generated a
series of large-scale topographic features, including Andeanstyle mountain ranges, foreland and backarc basins, and belts
of magmatism. All these would have led to major changes in
the vegetation and the fauna, even in birds. It is likely that
early ratites could fly (Mitchell et al. 2014a), but despite the
fact that they can fly, most birds are ‘extraordinarily sedentary’
(Mayr 1940). (For other, similar quotes from very experienced
ornithologists, see Heads 2012a, p. 278).
The Whitsunday–Median batholith belt runs through the
middle of New Zealand and along eastern Queensland. (In
contrast, subsequent rifting took place between New Zealand
and Australia). Thus, its location and its timing (Early
Cretaceous, following the separation of ostriches and of rheas)
together suggest that its development divided the Indo-Pacific
Gondwana
continental crust
Australides
Panthalassa
oceanic crust
Fig. 3. The Australides orogen, developed by subduction of Panthalassa crust beneath
Gondwana (movement of Panthalassa crust indicated by arrow; from Vaughan et al. 2005, and
Milani and de Wit 2008).
250
Australian Systematic Botany
M. Heads
New Guinea
continental crust
Whitsunday Volcanic
Province and Median
Batholith; active until
end of Early Cretaceous
Rifting; beginning in
Late Cretaceous
Queensland and
Marion Plateaus
W New Zealand
Australia
E New
Zealand
90 Ma
East Antarctica
West
Antarctica
Fig. 4. A reconstruction for 90 Ma showing the Early Cretaceous Whitsunday–Median
batholith silicic volcanic province and zones of Late Cretaceous rifting (Mortimer et al. 2005).
(From Heads 2014, reproduced with permission of Cambridge University Press.)
clade of ratites into kiwis and allies around the Indian Ocean,
and moas and tinamous around the Pacific basin. Overlap of
the two clades has developed subsequently, but only within
mainland New Zealand.
The break between emus (Dromaiidae) and cassowaries
(Casuariidae)
Emus and cassowaries, both living and fossil, are allopatric for
the great majority of their range, with minor local overlap in
north-eastern Queensland (Fig. 2). (A fossil cassowary
tibiotarsus, Casuarius lydekkeri, was thought to have been
found at Wellington Valley in New South Wales, but its
provenance has been questioned; it is perhaps more likely to
be from the Darling Downs in Queensland, 200 km west of
Brisbane; Worthy et al. 2014).
In traditional biogeography, groups in New Guinea have
dispersed there from either Asia or Australia. In this model,
New Guinea cassowaries have dispersed from Australia,
rather than evolving in situ from a widespread, generalised
cassowary–emu ancestor. Yet a dispersal model would imply
that the New Guinea cassowary species are all nested
phylogenetically in the Australian population, and this is
unlikely.
The overall allopatry between emus and cassowaries is
impressive and can be explained by vicariance, with the
minor overlap explained by local dispersal. The allopatry
around a break in eastern Queensland is a very common
pattern; for example, it occurs in marsupials, between
Dendrolagus of New Guinea and north-eastern Queensland,
and Petrogale, widespread through mainland Australia (Heads
2014, fig. 4.10).
In the traditional model, the differentiation between
cassowaries and emus is ecological; cassowaries live in
tropical rainforests, emus in drier habitats. However,
cassowaries live in cold (montane) rainforest, as well as in hot
rainforest. There is plenty of cold rainforest in south-eastern
Australia, similar to that in montane New Guinea; however,
(apart from the dubious record of C. lydekkeri) cassowaries
are not recorded there. There are also large areas of dry, open
grassland and savanna in New Guinea (especially in the Fly
River area), where there are no emus, only cassowaries. Thus,
cassowaries are well known from savanna and grassland
(Davies 2002), but are absent from this type of vegetation in
Australia; emus live in savanna and grassland, but are absent
from this type of vegetation in New Guinea. In any case,
aridification in Australia began only in the Miocene (Davis
et al. 2013), whereas Oligocene fossils from Riversleigh in
north-western Queensland) are already recognisable as emus
(Dromaiidae) rather than cassowaries (Mayr 2009; Worthy
et al. 2014).
Thus, simple ecological sorting does not explain the
phylogenetic and distributional break between cassowaries and
emus. An alternative idea is that emus occupy open habitat
because they are in Australia; they are not in Australia because
they favour open habitat. Likewise, cassowaries are mainly in
rainforest because they are a New Guinea group, and currently
New Guinea is mainly covered in rainforest. The original
differentiation between emus and cassowaries is attributed
here to the final phases of activity in the Whitsunday volcanic
province, at ~100 Ma (mid-Cretaceous), followed by rotation
of New Guinea away from Australia (Zirakparvar et al. 2013).
This implies that the original emu–cassowary clade dispersed
north across the Whitsunday-Median batholith belt before the
Panbiogeography, its critics, and the case of the ratite birds
last active phases along the belt led to the differentiation of the
two families.
A vicariance model for ratite evolution
To summarise, the following sequence can be proposed for the
main nodes in the ratite phylogeny and the tectonic events that
coincide spatially with them:
(1) Break between ostriches in Africa and their Indo-Pacific
sister group. Opening of Mozambique Channel at 160 Ma
(Late Jurassic).
(2) Break between rheas and Clades 3–5. The last pulse of Chon
Aike volcanism (138–157 Ma, latest Jurassic–earliest
Cretaceous).
(3) Break between the Indian Ocean clade (3) and the Pacific
clade (4). Rangitata orogeny and earlier phases of
emplacement of the Whitsunday–Median batholith
igneous province at ~130 Ma (Early Cretaceous).
(4) Break within the Indian Ocean clade (3), between the
Madagascar-New Zealand group and the Australia–New
Guinea group. Seafloor spreading around India plus
continued activity in Median batholith, at ~130 Ma (after
Node 3, but before separation of Madagascar–India from
Antarctica–New Zealand, especially after ~120 Ma) (Early
Cretaceous) (Reeves 2014).
(5) Break between emus and cassowaries. Last active phases
of magmatism in Whitsunday volcanic province at ~100 Ma
(mid-Cretaceous).
(6) Break within the Pacific clade (4), between the moas of
New Zealand and the tinamous of South America.
Opening of basins around New Zealand at 84 Ma (Late
Cretaceous).
This vicariance model of ratite evolution begins with a
global ancestor, and so there is no need for intercontinental
dispersal in any of the ratite clades themselves, only minor
overlap within continents. The overlap of moas and kiwis in
New Zealand occurred after their origin, but before strike-slip
displacement on the Alpine fault (starting in the Miocene)
caused species-level differentiation in each, as discussed
below.
The vicariance model incorporates all of the available
evidence from both the fossil and extant records. Most of the
data is from the extant record because the fossil record of
ratites is poor. With respect to Lithornithidae, in a vicariance
model, the common ancestor of the extant ratites already
occupied Europe and North America before lithornithids
differentiated as such. The precise mode of origin of the
family – its break with its sister-group – is unclear, because
the family’s affinities are not known.
The panbiogeographic approach, as illustrated here, explains
allopatry by vicariance and overlap by dispersal. Extinction is
another factor, but happens everywhere, all the time, and so
does not account for the neat, mosaic patterns of allopatry that
are observed in practice. For example, in the ratites, the global
allopatry of the clades is the dominant pattern. The comparatively
minor areas of overlap can be explained by dispersal. The
absence from India and the Antarctica mainland (living and
fossil) is probably the result of extinction. The absence from
Australian Systematic Botany
251
New Caledonia and all the Caribbean islands is perhaps
more enigmatic (Grenada is just 100 km from Trinidad, where
there are tinamous, and these can fly; Cuba is just 200 km from
the Yucatán Peninsula, where tinamous also occur).
Some further aspects of distribution in New Zealand are
discussed next, and illustrate panbiogeographic analysis at a
smaller geographical scale.
Kiwis (Apterygidae)
The trans-Indian Ocean clade of ratites includes a subgroup
comprising the kiwis (Apterygidae), endemic to New Zealand,
and their sister-group, the extinct elephant birds
(Aepyornithidae), only known from Madagascar. Mitchell
et al. (2014a) attributed the disjunction to long-distance
dispersal, but did not examine whether or not it is a standard
pattern.
In ducks, a widespread New Zealand clade (Anas chlorotis,
A. aucklandica, A. nesiotis and the extinct A. chathamica) is
sister to A. bernieri of Madagascar (Mitchell et al. 2014b).
Likewise, the beetle family Chaetosomatidae is known only
from Madagascar and New Zealand (Leschen et al. 2003).
In plants, the New Zealand species Euphorbia glauca
(Euphorbiaceae) is sister to E. emirnensis of Madagascar
(Riina et al. 2013). (It is possible that unsampled species such
as E. borbonensis of Réunion and E. reineckii of Samoa also
belong to this group; however, this would have little effect on
the overall pattern.) Korthalsella salicornioides (Viscaceae) is
in Madagascar, New Zealand and New Caledonia (Aubréville
et al. 1967; Molvray 1997).
New Caledonia is part of the same continental block as
New Zealand (Zealandia), and the biota includes several
connections with Madagascar (Heads 2010, supplement). The
terrestrial isopod Pyrgoniscus is in Kenya, Tanzania,
Madagascar, Lord Howe Island and New Caledonia.
(Schmalfuss 2003). Acridocarpus (Malpighiaceae) comprises
~30 species of Africa and Madagascar, and one disjunct
species endemic to New Caledonia that is sister to two
Madagascan species (Davis et al. 2002). Thus, the same
Zealandia–Madagascar pattern occurs in ratites, ducks,
crustaceans, beetles and plants, fulfilling one of the
preconditions for a vicariance model. The component groups
in the pattern all have very different ecology and means of
dispersal, suggesting that neither factor is responsible for
the pattern. In the model for ratites proposed above, the
Madagascar and New Zealand sister-groups differentiated in
Early Cretaceous time.
The kiwis (Apteryx) comprise two main clades, ‘brown’
and ‘spotted’. Members of the brown kiwi clade show very
high levels of genetic structuring, with mitochondrial DNA
haplotypes often restricted to local populations (Shepherd
et al. 2012). Sequencing studies of extant and subfossil
populations showed that the brown kiwi clade comprises two
main allopatric groups, with their mutual boundary at the
Alpine fault, not at the main watershed ridge of the Southern
Alps (Fig. 5; Shepherd et al. 2012; Heads 2014).
Baker et al. (1995) suggested that the ancestral brown kiwi
population moved north from Fiordland to Haast and then
Okarito, where the population diverged, yet this does not
252
Australian Systematic Botany
M. Heads
explain the cause of the divergence. It could be accounted for if the
ancestral brown kiwi population was already widespread through
New Zealand before the split. The main phylogenetic break
occurs between populations of the southern Apteryx australis
clade at the Arawata Valley and Haast Range (near Haast village;
Holzapfel et al. 2008), and members of the northern A. mantelli
clade at Okarito. The location of the break coincides with the plate
boundary, represented by the Alpine fault, and this has not been
recognised in prior studies. Most populations of the southern
A. australis group lie south-east of the main geographic divide.
However, the population at Haast and many in Fiordland lie west
of the main divide (and east of the Alpine fault; Fig. 5), and so the
main divide does not correspond with the phylogenetic break.
Wallis and Trewick (2009) discussed the basal split in the
brown kiwi clade and accepted that it was too old to reflect
Pleistocene events, such as glaciations. They suggested that it
could have been caused by uplift of the Southern Alps, but
if the break were due to uplift it would be located at the
main divide, not at the fault. In addition to the vertical
displacement, large-scale strike-slip (horizontal) displacement
has also occurred along the fault, and the observed pattern
suggests that this has caused the differentiation. Disjunction
A. mantelli clade
along the Alpine fault is now documented in more than
200 plants and animals, including kiwis (Heads 1998;
M. Heads, pers. obs.). For example, three species in the alpine
plant Abrotanella (Asteraceae) each show a major disjunction
along the fault (Heads 2012c).
Moas (Dinornithidae)
The other New Zealand ratites are the moas, giant birds that
became extinct in historical times. There are two main clades,
namely, the upland genus Megalapteryx, with most records at
900–2000-m altitude, and the remaining five genera, usually
found at lower sites (Bunce et al. 2009, fig. 2).
Molecular studies of subfossil material have supported the
idea that moa populations persisted in many refugia during
the Pleistocene glaciations, even in colder, montane areas. For
example, Megalapteryx shows high levels of genetic diversity
relative to the other genera, and this ‘likely relates to the
persistence of upland/montane habitat during both glacial and
interglacial periods’ (Bunce et al. 2009, p. 20 650). With
respect to the Oligocene marine incursions that flooded
parts of New Zealand, Bunce et al. (2009, p. 20 649) agreed
that ‘the survival of many endemic vertebrates preserved as
early Miocene fossils strongly argues against total
submergence’. Both kiwis (Worthy et al. 2013) and moas
(Tennyson et al. 2010) are known from early Miocene fossils
in central Otago.
Megalapteryx shows deep phylogenetic divisions with four
distinct clades, all in the South Island (Fig. 6; Bunce et al.
2009). The clades are allopatric, with one each in Fiordland,
Otago, Nelson and Marlborough–northern Canterbury. The
Fiordland clade is sister to the clade in Nelson, and so the
pattern is compatible with Alpine fault displacement. Bunce
et al. (2009) thought the break between the Fiordland and
Nelson Megalapteryx was caused by Pleistocene glaciations,
but Megalapteryx favoured colder, upland habitat, and so,
during colder phases, its range would probably have expanded
†
†
Megalapteryx
†
1 (2 (3 + 4))
†
4. Nelson
Okarito
†
Haast Ra.
main
divide
Alpine
fault
Fiordland
2. Marlborough
Alpine fault
main
divide
A. australis clade
†
Apteryx clade
(brown kiwis)
Fig. 5. The two clades of brown kiwi: Apteryx australis species group
(light grey) south-east of the Alpine fault, and A. mantelli species group
(dark grey) north-west of the fault. Dagger symbols indicate sequenced,
subfossil samples from populations now extinct (Shepherd et al. 2012).
(From Heads 2014, reproduced with permission of Cambridge University
Press.)
x
x x
SOUTH
ISLAND
3.
Fiordland
1. Otago
Fig. 6. The four clades of the moa genus Megalapteryx (Bunce et al.
2009). Localities with unsequenced fossils as X symbols (Worthy 1997).
Panbiogeography, its critics, and the case of the ratite birds
rather than contracted. Bunce et al. (2009, supporting
information, p. 2) acknowledged that ‘the phylogeographic
distribution of the Megalapteryx clades does not match
their phylogenetic relationships’. This is because the Fiordland
clade is sister to the Nelson clade (disjunct along the Alpine
fault), not the adjacent Otago clade. The pattern is consistent
with the Fiordland + Nelson population and the Otago
population breaking apart before the Alpine fault split the
Fiordland + Nelson clade.
It might be objected that the recent divergence date
between Megalapteryx and the other moas calculated by
Bunce et al. (2009), 5.8 Ma, rules out Alpine fault disjunction.
Nevertheless, this date is fossil-calibrated and so represents a
minimum clade age. For example, the calibrations employed
by Bunce et al. (2009, supporting information) include:
‘Casuariidae (emu v. cassowary). Normal distribution, median
at 25.5 Ma [the oldest emu fossil date], 95% range from 16 to
35 Ma.’ In other words, the maximum possible age of emu and
cassowary is stipulated as a ‘prior’, before any analysis, as 35 Ma
(with 95% credibility), no more than 9.5 million years older
than the oldest fossil in the group. But why 35 Ma? Why not
36 or 37, or 47, or 67 Ma. . .? The date is arbitrary. (For
more details on Bayesian dating, see Heads 2012b.) Thus,
although the topology of the Bunce et al. (2009) phylogeny is
of great interest, the fossil-calibrated dates cannot be accepted
as maximum clade ages.
A casual observation might suggest that the distributions
of the Megalapteryx clades reflect current climate, with the
western clades occurring in the wet forests to the west of the
Southern Alps and the eastern clades found in drier areas east of
the mountains. However, the pattern is not that simple. For
example, the eastern Clade A is recorded in areas (south of the
Nelson lakes, for example) that are wetter than substantial areas
occupied by the western clade B + C (north of the Nelson lakes,
for example). The sampling in the study by Bunce et al. (2009)
could be improved, but the Megalapteryx clades already appear
to be a typical case of Alpine fault disjunction, as in brown kiwis
(see above).
Conclusions
To summarise, none of the criticisms of panbiogeography
can be substantiated. It is not creationist, it does not ‘reject
dispersal’, its analyses are not ‘disingenuous’, and it does not
ignore or misrepresent key evidence. Panbiogeographic methods
have incorporated recent advances in geological knowledge,
produced new analyses of molecular and morphological
variation over space and time, and led to bold, new, testable
predictions. In contrast, the critics have overlooked recent
developments in geology, ignored many implications of the
molecular phylogenies, avoided confronting issues such as
the problem of the priors, and produced only timid variations
of the Modern Synthesis.
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