BiologzcalJournul of the Linnean Society (1996), 58: 325-342. With 6 figures
Biogeographic patterns and the evolution of
eureptantic nernerteans
M I K A E L HkRLIN
Department of<oology, Goteborg Univenip, Medicinaregatan 18, S-413 90 Gokborg, Sweden
Received 9 M y 1995, accqtedfor publication 18 Augurt 1995
The origin and evolution of the eureptantic nemerteans is discussed from a biogeographic point of view.
It is most likely that East Indian Ocean was part of the ancestral distribution of the Eureptantia. The
area cladogram estimated by Brooks parsimony analysis (BPA) is to a high degree congruent with a
vicariance explanation of the evolution of the Eureptantia and suggests an ancestral distribution
concordant with the Tethys Sea. A general area cladogram based on a combined BPA analysis of
eureptantic nemerteans and acanthuroid fishes is reconstructed and suggested as a hypothesis of the
relationships between east Indian Ocean, west Indian Ocean, west Pacific Ocean, east Atlantic Ocean,
west Atlantic Ocean, and the Mediterranean. This tree is compared with cladograms from the same
areas based on other taxa.
01996 The Linnean Sorirty of London
ADDITIONAL KEY WORDS: -cladistic biogeography
evolution BPA Nemertea Hoplonemertea.
~
~
~
ancestral area analysis
-
parsimony
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CONTENTS
Introduction . . . . . . . . . . . . . . . . .
Phylogeny and taxonomy of Eureptantia . . . . . . .
Biogeographic analyses . . . . . . . . . . . . . .
Endemic areas . . . . . . . . . . . . . . .
Ancestral area analysis . . . . . . . . . . . .
Area cladograms . . . . . . . . . . . . . .
Results . . . . . . . . . . . . . . . . . . .
Ancestral area analysis . . . . . . . . . . . .
Area cladograms . . . . . . . . . . . . . .
Discussion . . . . . . . . . . . . . . . . . .
Methodological considerations . . . . . . . . .
Origin and cladistic biogeography of the Eureptantia .
Towards a general reduced area cladogram of the oceans
Summary . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . .
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34 1
34 I
INTRODUCTION
Areas of origin (ancestral areas) and historical biogeography are fields that have
intrigued and fascinated systematists for a long time. Dispersal scenarios and
vicariance patterns are common features of biogeographic discussions with the aim
00244066/96/070325+18 $lt).OO/O
325
01996 The Linnean Society of London
326
M. H & U N
to explore to what extent the organisms’ active movements are the cause of their
diversification (dispersal) and to what extent geological movements on the earth or
other external causes are responsible (vicariance). Two major fields can be
recognized in biogeographic analyses: one concerns the origin and evolution of a
given clade, the other seeks general patterns in the evolution of biotas. In other
words, the first approach asks the question ‘where and how has this clade evolved?’
and the second asks ‘what relationship exists between these biotas?’. With the
development of cladistic or phylogenetic systematics both of these approaches to
biogeography have become more explicit. Based on a phylogenetic tree of the
studied group(s) a reduced area cladogram is constructed using one of several
methods (e.g. component analysis (Page, 1988, 1993), Brooks parsimony analysis
(Wiley, 1988; Kluge, 1988; Brooks, 1990), three-area statement analysis (Nelson &
Ladiges, 1991)). All of these methods maximize the vicariance property of
biogeographic explanation and minimize the dispersal property in much the same
manner as phylogenetic analysis maximizes homologies and minimizes homoplasies.
The main concern of these methods is the study of correlated patterns from
independent taxa inhabiting the same areas (e.g. Nelson & Platnick, 1981;
Humphries & Parenti, 1986),with the aim of obtaining a general pattern of an area
history. Information from as many independent clades as possible is thus considered
important. Bremer (1992) brought back the focus to the study of the origin and
evolution within a single clade. He developed a method to estimate how liely it is
that a certain area inhabited by extant species was part of the ancestral area.
Analysing the geographic distribution within a clade from a historical perspective
contributes to the knowledge of the evolution of the group and have the potential to
enhance the general understanding of the evolution of biotas.
In this paper I discuss the origin and evolution of the eureptantic nemerteans from
a biogeographic perspective. I base this discussion on an ancestral area analysis
(Bremer, 1992) and an area cladogram produced from the phylogenetic hypothesis
in Harlin & Sundberg (1995). The results from the eureptantic nemerteans are also
discussed and compared with area cladograms based on marine water striders
(Andersen, 1991) and corals (Wallace et aL, 1991) from the same region. In
connection with this I present an area cladogram based on a combined data set of
eureptantic nemerteans and acanthuroid fishes (Winterbottom & McLennan, 1993).
Hence, the aim is to present a hypothesis of the origin and evolution of the
Eureptantia but also a biogeographic hypothesis of the involved areas.
PHnOGENY AND TAXONOMY OF EUREFTANTIA
The 43 described eureptantic nemertean species are traditionally grouped into
nine families and 22 genera, many of them monotypic. They are furthermore divided
into the two taxa Aequifurcata and Inaequifurcata based on the structure of the
cerebral sense organs. Harlin & Sundberg (1 995) presents a phylogenetic hypothesis
of these species which indicates that many of the taxa are non-monophyletic. A few
species are excluded from the analysis due to inadequate descriptions. All six most
parsimonious trees resulting from this analysis are highly congruent (Fig. l), the only
variation is in two of the minor terminal clades. Despite a rather low (0.20) adjusted
consistency index (Klassen, Mooi & Locke, 1991), not significantly lower than in
animal and plant taxa in average though (Sundberg & Svensson, 1994), the new
CIADISTIC BIOGEOGRAPHY OF THE EUREPTANTIA
327
hypothesis is preferred over the old for several reasons. It is the only explicit
phylogenetic hypothesis of the group and compared with the traditional classification, the hypothesis (Fig. 1) proposed by Harlin & Sundberg (1995) is 16 steps shorter
using the same set of characters in a constrained analysis of the old classification.
Members of the Eureptantia are found world-wide with a concentration of the
distribution in the-Indo-Pacific and the Mediterranean. Closely related taxa show a
disjunct distribution (Fig. l), i.e. they are vicars of one another. Similar observations
was known long before Darwin wrote about vicariance in 1859 and the fact that the
distributions of organisms are clustered into areas of endemism is strong evidence
that biotas are historically structured (Cracraft, 1994).
3
f-I
I
6
%631
Figure I . Phylogenetic hypothesis of the eureptantic nemerteans. Redrawn from Harlin & Sundberg
(1995).The geographic area is noted after each species. WP = Western Pacific, WIO = Western Indian
Ocean, EIO = Eastern Indian Ocean, EAT = Eastern Atlantic Ocean, WAT = Western Atlantic
Ocean, and ME = Mediterranean. Areas within brackets are the less inclusive ones (Gbr = Great
Barrier Reef). Terminal branches and internal nodes are numbered. This tree is used as data for the
biogeographic analyses.
328
M.W L I N
BIOGEOGRAPHIC ANALYSES
Several approaches exist for analysis of biogeographic data, many are closely
linked to cladistic philosophy although based on slightly different assumptions. The
purpose with this study is 2-fold; to study the biogeographic evolution within
Eureptantia and to use these results for a comparison with other studies to reach a
general hypothesis of the relationships of the concerned biotas. For the first purpose
I use Bremer’s (1992) ancestral area analysis and Ronquist’s (1994) method to
identify an ancestral area(s) or place(s) of origin of the eureptantic nemerteans and
Brooks parsimony analysis (BPA) to reconstruct a reduced area cladogram of the
involved areas. Besides serving as tool in the study of the evolution of the
Eureptantia, the reduced area cladogram is used for a general biogeographic
hypothesis as discussed below. Both BPAs and ancestral area analyses are analysed
with PAUP 3.1.1. (Swofford, 1993) and MacClade 3.0 (Maddison & Maddison,
1992) and are described below. The trees are compared with results obtained by
Component 2.0 (Page, 1993).
Endemic areas
A cladistic biogeographic model requires at least one endemic species in each area
under consideration (Humphries & Parenti, 1986; Harold & Mooi, 1994). I
recognize five such areas (described below) within the eureptantic nemerteans. Some
contain several minor areas that could be recognized as well. These are mentioned
under the appropriate more inclusive area. Correspondence between the different
area subdivisions is also illustrated in Figure 1.
Eastern Indian Ocean (EIO)
This area includes the Indonesian archipelago (Timor, Savu, Sumba, Flores,
Ambon, Seram, Obi, Sulawesi, Tiur) and is inhabited by several endemic species.
Wallace et al. (199 1) also recognized this area. Andersen (1 99 l), on the other hand,
divided the area in to three subareas (Sulawesi, Philippine, Malayan). Species:
Drepanophorella sebae, Drepanophoria pajungae, Drepanophoringia waingapumk, Paradrepanophorus obimk, Drepanophorina argur, D. lata, D. savuensis, Punnettia wilhyana, Coella tiurensis,
Punnettia maldivensis, P. timorensis, P. cerina, Drepanophorus modestus, Drepanobanda
trilineata.
Western Indian Ocean (WIO)
Drepanophoresta rosea is endemic in the areas around the Maldives while Punnettia
wilhyana and hnnettia maldivmis also are known from the Indonesian archipelago and
thus scored in the EIO category as well. This area corresponds to the western and
central Indian Ocean area in Wallace et al. (199 1) and Andersen’s (199 1) Indian
Ocean area.
Western Pan& (wpl
Species found in the seas around New Guinea, Australia (Great Barrier Reef), and
New Caledonia are included in this category. All species known from this area are
endemic. The area corresponds to the Western Pacific area of Wallace et al. (1991)
and the three areas West Pacific, Papuasia, and Australian in Andersen (1991).
CLADISTIC BIOGEOGRAPHY OF T H E EUREFTANTIA
329
Species: Drepanophoresta l@ensis) Drepanophorim guineensis, Urichonemertes pilorhynchus,
Xaonemertes rhamphocephalus, finnettia micrommata.
Eastern Atlantic Ocean (EAT
Species known from the west coast of Norway (Uniporus hyalinus, Uniporus borealis,
and Uniporus acutocaudatus), the English Channel (Paradrepanophorus crassus) finnettia
spectabilis, and Punnettia sphdida). The former three species are endemic but the latter
three are also known from the Mediterranean.
Western Atlantic Ocean (WA7)
Species from the east coast of North America (Hubrechtonemertes lahsterz) and the
Caribbean (Curranemmertes natans) are scored in this category. Both are endemic.
Mediterranean (ME)
Next to the Eastern Indian Ocean (EIO), the Mediterranean is the area with most
known endemic species. Nine species are known at present. Most of these species are
only known from the Bay of Naples, Italy. A few are also found in other localities like
Banyuls, Marseille, Sicily and Trieste. Three species are also known from the English
Channel. Species: Bepanogigas albolineatus, Paradrepanophorus corallinicola, P. n d h , P.
crc1ssus, finnettia splendida, P. spectabilis, P. hubrechti, Bepanophorus rubrostriatus, Brinkmannia mediterranea.
Ancestral area anabsis
Bremer (1992)developed a method for analysis of geographic distributions within
a clade, treating each geographic area as a binary character in a parsimony analysis.
The method estimates how likely it is that a certain area inhabited by extant clade
members was part of the ancestral distribution, supposing that the latter was smaller
than the recent distribution of the clade. Following Bremer I have first considered the
null-hypothesis in vicariance biogeography which says that the ancestral distribution
of a taxon equals its present geographic distribution (i.e. all areas inhabited today
were ancestral). This accommodates the option that all areas were inhabited from the
start and later lost or kept their inhabitants in one way or another. All necessary
losses (1- > 0) are optimized on the cladogram using reversed Camin-Sokal
parsimony (‘irreversible down’ option in PAUP) and not allowing any reversions.
The result from this is listed in the L column (Tables 1 and 2). The alternative to the
above mentioned scenario is that none of the present geographic areas were part of
the ancestral distribution of the clade. In this case all species must have entered into
these areas later. Optimizing all necessary gains under ‘normal’ Camin-Sokal
parsimony (‘irreversible up’ option in PAUP) gives a measure of this scenario (Tables
1 and 2, column G). Bremer’s method thus takes both these aspects into account and
use a quotient between the two as a measure of how likely it is that a specific area
was part of the ancestral distribution. The G/L quotients are considered as such a
measure; the higher the value, the more likely it is that the area was part of the
ancestral area (AA). These values are rescaled to values between zero and one (AA)
by dividing all G/L values with the largest G/L value. The cladogram in Figure 1
is used as base for the ancestral area analyses.
330
M. m
N
Area cludograms
An area cladogram illustrates the relationships among areas or biotas as inferred
from phylogenetic data of organisms. Unique occurrences of taxa and their
successive diversification in the tree are explained in terms of vicariance while a
homoplastic pattern of the taxa need explanations in terms of dispersal or extinction.
In a BPA both terminal and internal nodes in the phylogenetic tree are used for
information; areas are coded as absent or present in these parts of the tree. A BPA
is a parsimony analysis where the terminal taxa and internal nodes (clades)are binary
characters and the areas are taxa (Kluge, 1988; Wiley, 1988; Brooks, 1990).
Terminal species present in more than one area, widespread species, are often
considered problematic in biogeographic analyses. One possible cause for this can be
the confusion surrounding the species concepts. The basic assumption in biogeographic analyses must be to view species as monophyletic taxa (e.g. Mishler &
Donoghue, 1982) and their potential informativeness evaluated in a congruence
analysis (see discussion). Thus, I have considered widespread terminal species as
potential synapomorphies in the BPAs. Other problems with BPA are treated in a
later section when the area cladograms are interpreted. The phylogenetic tree in
Figure 1 is used as the base for the biogeographic analysis of the Eureptantia. I have
performed two BPAs of the eureptantic nemerteans, the first with the five endemic
areas listed above and the second with the subareas of these more inclusive endemic
areas. The relationship between the more and less inclusive endemic areas is
illustrated in Figure 1.
One aim of historical biogeography is to use data sets representing independent
taxa to find general patterns among areas. Winterbottom & McLennan (1993)
presented a cladogram of the acanthuroid fishes with a geographic distribution
similar to the one shown by the Eureptantia. I have used the information from the
cladogram in Winterbottom & McLennan (1993) in a BPA and combined that with
the data from the eureptantic nemerteans. Slight differences exist between the
matrices; in the acanthuroid fishes matrix the area eastern pacific (EP) is present
while missing in the eureptantic matrix and in the eureptantic matrix the area
Mediterranean (ME) is present while missing in the acanthuroid matrix. Missing
areas are denoted a question mark (?) in the specific section of the combined matrix
as suggested by Wiley (1988) among others. In the eureptantic matrix the Indian
Ocean is divided into an eastern and western part, and subsequently, the
acanthuroid fishes present in the Indian Ocean are coded as present both in the
eastern and western part of the ocean. The cladogram in Figure 1 is the source for
eureptantic BPAs and the acanthuroid data is incorporated into the eureptantic
matrix for the combined analysis.
In the present study I have considered two options for rooting area cladograms.
First, I have considered an hypothetical all zero outgroup which is suggested in, for
instance, Wiley (1988) and Cracraft (1994). Second, the result from the ancestral area
analysis was used to root the tree. Results from both options are discussed.
CLADISTIC BIOGEOGRAPHY OF THE EUREPTANTIA
33 I
RESULTS
Ancestral area analyk
The analysis identifies eastern Indian Ocean (EIO) as the most likely ancestral
area (Table I), or rather that it was likely that EIO was a part of the ancestral area.
EIO has an M-value of 1 (G/L = 0.80) while the closest competitor, the
Mediterranean (ME) have an AA-value of 0.72. The other areas were less likely to
be part of the ancestral area. It is worth noticing that it is not the area present in the
most ‘basal’ clade in the tree that is most likely to be part of the ancestral area;
something that simply looking at the tree might have suggested. A similar approach
was criticized by Maddison, Ruolvo & Swofford (1992) who pointed out that
“parsimony considers the entire tree structure, not just that of the basal clade, and
thus clades beyond the basal clade must be examined to determine the most
parsimonious ancestral state”. However, optimizing geographic distribution as one
multistate character (Fig. 2) in the tree and looking for the ancestral state at the base
of the tree presents several equally parsimonious reconstructions in this case; thus, it
does not help to solve the question. If the outgroup used in Harlin & Sundberg (1995)
is added (Siboganemertes weben), which is present in EIO, then the optimization
identities EIO at the root of the tree. The ancestral area analysis, however, helps to
resolve the ambiguities in Figure 2 without using an outgroup.
In the analysis with less inclusive areas (Table 2) the most likely ancestral area is
the Mediterranean (AA = 1, G/L = 0.58). Other areas with comparatively high
M-values are Timor (AA = 0.57), EAT (0.43), Maldives (0.36) and Flores (0.34).
The results of this analysis shifts towards a hypothesis indicating a more likely origin
in the ME/EAT rather than in the EIO. Areas in the EIO like Timor and Flores stid
have rather high values even though the results are almost opposite the results from
the analysis with more inclusive areas (Table 1). Depending on the inclusiveness of
the areas used, the likely origin (ancestral area) of the eureptantic nemerteans is
either a Indo-Pacific one, or, one in the Mediterraneadeast Atlantic Ocean.
Area cladogram
The BPA of the eureptantic nemerteans resulted in one most parsimonious area
cladogram with a consistency index of 0.87 and a retention index of 0.64 (Figure 3).
The tree distribution is significantly skewed to the left (81 = -0.822) according to
Hillis & Huelsenbeck (1992). The tree is rooted with an all zero outgroup. Using
EIO, which is the most likely area to be part of the ancestral area according to Table
1, shifts the topology. However, since the result from the ancestral area analyses
varies depending on the inclusiveness of the areas used I prefer to root the tree with
an all zero outgroup. The reduced area cladogram in Figure 3 indicates two major
sister-faunas; one Indo-Pacific and one Mediterranean / east Atlantic Ocean. With
Component 2.0 one optimal tree is found when ‘leaves added‘ are minimized and
the NNI searching algorithm is used. The same tree is obtained whether or not
widespread associates are mapped or not (i.e. both under assumption 0 and 1). This
tree differs from the one in Figure 3 in the clade comprising WP, EIO and WIO. The
Component tree suggests a relationship like (WP (EIO, WIO) rather than (WIO
(EIO, WP).
332
M. M L I N
Using the less inclusive areas (within brackets in Fig. 1) the BPA of the eureptantic
nemerteans results in two equally parsimonious trees with a consistency index of
0.82, a retention index of 0.88 and a gl of -0.637. One of these two trees is shown
in Figure 4 and rooted with an all zero outgroup. This analysis supports the results
from the analysis based on the more inclusive areas indicating two sister-faunas.
Monophyletic Indo-Pacific faunas are present as are a Mediterranean / east Atlantic
Ocean fauna.
Combining the eureptantic BPA matrix with one extracted from the acanthuroid
fishes in Winterbottom & McLennan (1993) results in three equally parsimonious
area cladograms with a consistency index of 0.89, a retention index of 0.76 and a gl
value of -0.717 (significantly skewed to the left). The strict consensus tree (rooted
with an all zero outgroup) of these trees is illustrated in Figure 5 . The variation
I
I
M
Emlvvlo
EAT
WAT
D W P
=polymorphic
Eequivocal
Figure 2. The geographic distribution plotted onto the cladogram as one multistate character with six
states. The equivocal state of the ancestral area is caused by the many equally parsimonious
reconstructions. Abbreviations as in Fig 1.
CLADISTIC BIOGEOGRAPHY OF THE EUREPTANTIA
333
TABLE1. Estimation of ancestral areas of Eureptantia. G=number of necessary gains under
forward Camin-Sokal parsimony. L=number of necessary losses under reverse Camin-Sokal
parsimony. AA=G/L quotients rescaled to a maximum value of 1 by dividing with largest G/L
value. The S values are number of steps under reversible parsimony. RF' values are S values
rescaled to a maximum value of one by inverting them and multiplying by the smallest S value.
Area
G
L
G/L
AA
S
RP
Eastern Indian Ocean (EIO)
Mediterranean (ME)
Eastern Atlantic Ocean (EAT)
Western Pacific (WP)
Western Indian Ocean (WIO)
Western Atlantic Ocean (WAT)
12
7
4
5
3
2
15
12
16
20
14
14
0.80
0.58
0.25
0.25
0.21
0.14
1
0.72
0.31
0.31
0.26
0.18
19
19
19
20
20
20
1
1
1
0.95
0.95
0.95
among these trees is in the clade comprising the Mediterranean, eastern Pacific
Ocean and east Atlantic Ocean. The tree is congruent with the tree based only on
the Eureptantia (Fig. 3). For comparative purposes a majority rule consensus tree of
the three area cladograms obtained based solely on the Acanthuroid tree is illustrated
in Figure 6. Using the same settings as in the Eureptantic matrix, Component finds
the same tree as in the analysis based on the Eureptantia alone.
I have tested all area cladograms for deviation from randomness by calculating ten
sets of randomized characters (shuffle option in MacClade; keeping the character
state frequency intact). All randomized trees are longer, have lower CI, lower RI,
and are less skewed to the left than their original counter parts indicating that the
original trees have a higher hierarchical information content than trees generated
from a randomized data matrix. The results are summarized in Table 3.
TABLE2. Ancestral area estimation of the Eureptantia using less inclusive areas than in Table 1
Abbreviations the same as in Table 1.
Area
G
L
G/L
AA
S
RP
Mediterranean
Eastern Atlantic Ocean (EAT)
Timor
Indian Ocean (Maldives)
Flores
Ambon
New Guinea
Great Barrier Reef
Saw
Ceram
Western Atlantic Ocean (WAT)
Obi
Tiur
New Caledonia
Sumba
Sulawesi
7
4
4
3
1
2
2
2
2
1
2
1
1
1
1
1
12
16
12
14
5
13
15
15
18
11
14
15
15
15
17
18
0.58
0.25
0.33
0.21
0.20
0.15
0.13
0.13
0.11
0.09
0.14
0.07
0.07
0.07
0.06
0.06
1
0.43
0.57
0.36
0.34
0.26
0.22
0.22
0.19
0.16
0.24
0.12
0.12
0.12
0.10
0.10
21
21
22
22
22
22
22
22
22
22
22
22
22
22
22
22
1
1
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
0.95
M. H&LIN
334
DISCUSSION
Methodological considerations
Ancestral area analysis (Bremer, 1992) is a method designed to evaluate the
relative probability of certain areas being part of the ancestral distribution for a
clade. Ronquist (1994) criticized Bremer’s (1992) approach on the grounds that it
was too pattern oriented. The arguments were that pattern oriented methods
“...suffer from a high risk of producing unreasonable results [and] do not always
produce interesting results”. Instead Ronquist (1994) favoured a parsimony method
which allowed reversions and thus counted the steps (S in Table 1 and 2) for
1
El
0
3
til
f
!
i/
i
tE
1
2L1
A
B
I
6
12
5
15
a3
37
49’
30
28
61
9
21
16
2c
51
51
53
100
26
40
41
42
49
50
55-60
62-64
61
Figure 3. Reduced area cladograms fmm the BPA of Eureptantia using the areas in Table 1. The tree
is rooted with an all zero outarea. CI = 0.87 and RI = 0.64. The nodes (characters)from Fig. 1 are
plotted on the cladogram using DELTRAN optimization (preferringparallelisms(dispersal)over reversals
(extinctions)). Bold numbers indicate pardelism and an asterisk (*) indicates reversals. Bootstrap values
(100 replicates) are given as the larger, bold figures on the right hand side of the nodes.
CLADISTIC BIOGEOGRAPHY OF THE EUREPTANTIA
335
geography optimized as a multistate character, allowing all areas to be ancestral. He
then rescaled the S values to a maximum value of one by inverting them and
multiplying by the smallest S value; this value is called reversible parsimony (RP in
Table 1 and 2). Ronquist’s method produce results more or less concordant with the
ones obtained by Bremer’s method (cf. Tables 1 and 2). A multistate coding of the
character geography (Fig. 2) does not help solve the question in this particular case
because of several equally parsimonious reconstructions unless the outgroups used in
Harlin & Sundberg (1 995) are added. When the outgroups are added, the multistate
optimization is concordant with the results using Bremer’s method (i.e. a likely origin
in EIO). EIO is thus preferred as a hypothesis of most likely being part of the
ancestral area of the Eureptantia. Ronquist’s method is to be preferred over the
optimization in Fig. 2 since it is more decisive.
Besides being interesting in themselves, a possible application of the results from
an ancestral area analysis is as a means for rooting area cladograms. However, it can
be sensitive for the inclusiveness of the areas used and subdividing a more inclusive
endemic area into smaller subareas may alter the results. When EIO was subdivided
into less inclusive areas the analysis favoured the ME and EAT as ancestral rather
than EIO. Already in the analysis with more inclusive areas, however, the
Mediterranean was quite likely to be part of the ancestral area. The reason for a shift
37
I
47
I
48
I
Figure 4. One of the two most parsimonious area cladograms from the BPA of the eureptantic
nemerteans using the areas in Table 2. The only difference between the two trees is in the clade
comprising WAT, Great Barrier Reef and Tiur Island where WAT and Great Barrier Reef are sister
areas in the other tree. CI = 0.82 and RI = 0.88in the two trees. The numbers illustrate the same thing
as in Fig. 3.
M. H&UIN
336
like this can have several explanations. One can be that data are ambiguous, another
that the method is sensitive for the number of species in each area (as discussed
above). The latter of these causes has to be tested in each specific case. Just as it is
dimcult to compare the results from two phylogenetic data matrices with respect to
consistency indices or tree lengths it is dimcult to compare two different ancestral
area analyses. I have preferred the all zero outgroup since the results from the
ancestral area analysis are somewhat ambiguous. However, the ancestral area
estimates can serve as a tool when interpreting the area cladograms as discussed
below.
In a recent empirical comparison of component analysis, BPA and three-area
statements, Morrone & Carpenter (1994) conclude that “none of the computer
implementations of the methods compared proved to be more effective than the
other”. The purpose of the present paper is not to compare methods, but I have
checked the results obtained by BPA with Component 2.0 and the major results are
79
A
78
I
85
Figure 5. The strict consensus tree of three most parsimonious trees from the combined BPA based on
the eureptantic nemerteans and the acanthuroid fishes. CI = 0.89 and RI = 0.76 in the three trees.
Bootstrap (100 replicates) values given in bold at the nodes.
CLADISTIC BIOGEOGRAPHY OF THE EUREF'TANTIA
337
Figure 6. Majority rule consensus based on the three most parsimonious area cladograrns from the
Acanthuroid fishes.
TABLE
3. Tree statistics. Randomized values (* standard deviation) are given within brackets.
Matrix
Eureptantia
Acanthuroid fish
Combined
Length
77 (86k1.7)
20 (25*1)
97 (115k1.9)
CI
RI
gl
0.87 (0.78i0.02)
0.95 (0.75k0.03)
0.89 (0.75*0.01)
0.71 (0.44k0.05)
0.90 (0.54i0.07)
0.79*(0.43*0.04)
-0.82 (0.41i0.27)
-1.87 (-0.1 1k0.32)
-0.72 (0.32k0.20)
338
M. €L&LIN
similar as discussed above. However, the relative merits and philosophical
assumptions of the various existing methods for biogeographic analyses still need a
comprehensive review and evaluation, which is something that will have to be
addressed elsewhere.
Olligin and cludistic biogeogaply of the Etlreptantia
Stiasny-Wijnhoff(1925, 1926)discussed the distribution of some of the eureptantic
taxa, focusing on the Aequifurcata and Inaequifurcata and their relation to the
Tethys Sea. The Inaequifurcata have a world-wide distribution while the
Aequifurcata have a more restricted distribution (Mediterranean and the Indonesian
archipelago) where some species follow the same distribution as the traditional
Tethys Sea once had. However, that discussion is flawed partly because nonmonophyletic taxa are used. Most of the taxa discussed in these and subsequent
papers regarding the reptantic or eureptantic nemerteans have been accorded nonmonophyletic status by Harlin & Sundberg (1995).
The ancestral area analyses give two solutions to the most likely ancestral area.
When the more inclusive areas are used the EIO is most likely to be part of the
ancestral area and with the less inclusive areas the ME / EAT are most likely, i.e. two
opposing parts of the Tethys Sea are suggested. Optimizing geography as a
multistate character (Fig. 2) supports the EIO if the outgroup used in the
phylogenetic analysis (Harlin & Sundberg, 1995)is added. Furthermore, I have more
confidence in the more inclusive areas since the exact distribution of the species using
the less inclusive areas are poorly known. Therefore I prefer the hypothesis
suggesting EIO as the most likely ancestral area. The area cladogram in Figure 3
complements the ancestral area analysis in that it identifies two sister-faunas which
coincide with the two most likely ancestral areas. With a consistency index of 0.87
the area cladogram (Fig. 3) is congruent with a vicariance model, i.e. the splitting of
a clades ancestral geographic range into two or more sub-regions with subsequent
divergence of the clade in respective regions. However, there are a few instances that
require other explanations such as dispersal. Sober (1988) argues that the
relationship between phylogenetic and biogeographic analyses is analogous rather
than homologous since biogeographic analysis requires horizontal explanations of
homoplasies (dispersal) while phylogenetic analysis does not. Something has to be
minimized in order to reach a hypothesis. In the case of vicariance and dispersal the
only possibility is dispersal because there is no upper limit to what can be explained
with dispersal. Such explanations will never yield any generalizations. The horizontal
nature of dispersal does not dismiss it as an a postaiuri explanation in biogeography.
Excluding the possibility for parallelisms (dispersal), i.e. using a Dollo parsimony
(Page, 1994))yields a cladogram six steps longer than the tree in Figure 3 which is
based on a Wagner parsimony with unordered characters. Thus, a biogeographic
hypothesis of the Eureptantia is more parsimonious if parallelisms (dispersals) are
allowed.
I have plotted the nodes (characters) from Figure 1 on the area cladogram in
Figure 3 using DELTRAN optimization. DELTR4N delays the transformations
which means that parallelisms (i.e. dispersals) are preferred over reversals (i.e.
extinctions). Bold numbers indicate instances that require explanations other than
vicariance. Punnettia willeyana is a widespread species found in EX0 and WIO. It could
CLADISTIC BIOGEOGRAPHY OF THE EUREPTANTIA
339
have originated in either of these areas and then dispersed into the other. The most
likely scenario is an origin in EIO (as inferred from the ancestral area analysis, Table
1) with a subsequent dispersal to WIO. Another possible scenario is an origin in the
ancestral area of the Indo-Pacific clade (WP, EIO, and WIO) in Figure 3 and that
P. willqana never entered or went extinct in WP (an ACCTRAN optimization is
needed for that). The same scenarios are possible for Punnettia maldivmis and the
clade originating at node 37 (Drepanophorellasebae, Drepanophoria pajungae, Drepanophoringia waingapurnis, Drepanophorestu rosea) in Figure 1. Following the area cladogram in
Figure 3 and the results from the ancestral area analysis in Table 1 the most likely
origin for the genus Paradrepanophoms (node 40 in Fig. 1) is in the EIO with a later
dispersal to and diversification (node 41-42) in the ME and EAT. Clade 49
(Hubrechtonemertes lankesteri, Urichonemertes pilorhynchus, Coella tiurmk, Xmonemertes
rhamphocephalus, Curranemertes natans, Punnettia splendida, and Punnettia micrommata)
probably originated and went through a cladogenesis (node 49-40) in the ancestral
area of all modern oceans, but never entered WIO. Several cladogenetic events (51,
52 and 54) took place in connection with the vicariance of WP and EIO followed by
successive dispersals into WAT as suggested by nodes 5 1-53. A problem with BPA,
it is argued (Wiley, 1988; Page, 1994), is that ancestors and descendants sometimes
appear on the same node in the area cladogram. This is the case with the clade
supported by nodes 49 and 50 (Fig. 3). Similar situations appear in other parts of the
area cladogram. One possible explanation for such events is that a cladogenesis
happened on another geographic scale than the one studied which can be seen if the
area cladogram in Figure 3 is compared with that based on the less inclusive areas
(Fig. 4). For instances, characters 51-53 support two successive clades and one
terminal branch. Other causes are discussed by Page (1994). The analysis
distinguishes between widespread terminal taxa; two of the nodes (Paradrepanophoms
crassus and Punnettia splendida) are regarded as synapomorphies supporting the ME /
EAT cladogenesis while the other two (Punnettia willeyana and Punnettia maldivmis) are
viewed as homoplastic. The genus Drepanophorus (node 61) probably originated in
rubrostriatus).
EIO and later dispersed into ME (0.
The phylogenetic tree in Figure 1 is significantly asymmetric using two of the
statistics (R = 11.26 and dN= 5.24) in Kirkpatrick & Slatkin (1993) with most
statistical power for trees with more than 20 species. One explanation for asymmetric
trees could be that species living in geologically active areas experience frequent
vicariant events resulting in a biased cladogenesis. A possible cause for the
asymmetry in the eureptantic evolution could be that many species and other taxa
evolved in the south-east Asia, which is, and has been, a geologically active area. The
origin of south-east Asia can be traced back to the break-up of the Gondwana
continent. Hamilton (1988) argues that the crust of Sumatra was continental at the
end of Palaeocene, but probably already during Precambrium although no rocks of
that age have been identified. Sumatra belongs to the same magmatic arcs as does
the Malay Peninsula and may have been rifted from what is now medial New Guinea
in Middle Jurassic time while Java is entirely of post-Jurassic age (Hamilton 1988).
The sea between the lesser Sunda islands and the Mollucans, the Banda Sea, is dated
back to early Cretaceous (130 Mya-120 Mya). One hypothesis is that the floor of the
Banda Sea is a piece of the Tethys sea that became divided into WP and EIO
(Audley-Charles 1987, and references therein). This vicariance is probably not the
one reflected in the area cladogram (Fig. 3) between EIO and WP. The vicariance
between EIO and WP in Figure 3 is more likely a result of the origination of present
340
M.H&UIN
day Indonesia. Eastern Indonesia as it is known today originated when Australia
collided with the Asian volcanic arc (Banda) some 20 Mya (Audley-Charles, 1987).
When India (during Tertiary) collided with the Asian continent some of the small
oceanic marginal basins opened up (Baker, Hall & Forde, 1994).The eastern part of
the Tethys Sea was closed during the Miocene (20 Mya) while the connection with
the Atlantic Ocean closed 5-6 Mya (Boero & Bouillon, 1993).The strait of Gibraltar
once again connected the Mediterranean with the Atlantic Ocean 5Mya. During
this isolation of the Mediterranean (the Messinian crisis) it was almost completely
dried out and the salinity and temperature were very high, which made it hard for
many species to survive. The many autopomorphies on the EIO branch in Figure 3
indicate the high cladogenesis in that area during the last 20-30 million years.
Towards a general reduced area cludogram ofthe oceans
Parenti (1 99 1) used freshwater fish (sicydiine gobies) to estimate the relationships
between the modern oceans. The area cladogram was rather unresolved and the
only conclusion drawn was that vicariance between WP and EP preceded vicariance
between the Atlantic Ocean and EP. Parenti (199 1) also discusses a cladogram based
on stingrays and their helminth parasites (from Brooks, Thorson & Mayes, 1981)
which suggests a vicariance pattern like (Indo-Pacific (EP, Atlantic Ocean)). This
congruent with the BPA based on the eureptantic nemerteans and the acanthuroid
fishes. The combined BPA of the eureptantic nemerteans and the acanthuroid fishes
resulted in three most parsimonious trees which are summarized as a strict consensus
tree in Figure 5, which is in completely agreement with the area cladogram in Figure
3 based solely on the Eureptantia. These trees show the same divergence sequence
of WP, EIO and WIO as does the hypothesis in Wallace et al. (1991); (WIO (EIO,
WP)). This sequence is also supported by some geological data as mentioned above.
Andersen’s (1991) study of the marine water striders suggests the relationship (WP
(EIO, WIO)) translating his areas into the ones used in the present study. This
pattern is the same as obtained with Component 2.0 for the Eureptantia and the
combined matrix. However, the present study offers higher resolution of the
relationships between the modern oceans and can serve as a working hypothesis into
which more data can be incorporated.
Summary
The results from the biogeographical analyses presented here enhance the
understanding of the evolution of the eureptantic nemerteans since it suggests likely
places of origin and distinguish between vicariance and dispersal events. Many of the
eureptantic taxa evolved in the Tethys sea, most likely in the part that later became
EIO. Vicariance was probably important in the evolution of the Eureptantia as
indicated by the high codivergence between areas and taxa. Geologically south-east
Asia is one of the most interesting areas (Baker et al. 1994) and it would be very
interesting to study the distribution of the Eureptantia more carefully in that region
and compare with the evolution of the islands in the Indonesian archipelago. Such
studies have to await more knowledge of the eureptantic distribution within
CLADISTIC BIOGEOGRAPHY OF THE EUREPTANTIA
34 1
Indonesia, but the present study serves as a good starting point and working
hypothesis for future research.
ACKNOWLEDGEMENTS
I thank Mats Envall, Christoffer Schander, Per Sundberg, and Mikael Thollesson
for valuable comments on earlier drafts of this manuscript. The systematic discussion
group at Depts. of Zoology and Systematic Botany, University of Goteborg is
gratefully acknowledged. Drs Roderic D.M. Page and Daniel R. Brooks reviewed the
manuscript and I thank them for useful comments. This study was financially
supported by Lmnanders Foundation, Colliander, and by various funds of the Royal
Swedish Academy of Science.
REFERENCES
Andersen NM. 1991. Cladistic biogeography of marine water striders (Insecta, Hemiptera) in the Indo-Pacific.
Australian System& B o h y 4: 15 1- 163.
Audey-Charles MG. 1987. Dispersal of Gondwanaland relevance to evolution of the angiosperms. In:
Whitmore TC, ed. Bwgeogrphical euoluhn of ihe Malay archipelago. Oxford Clarendon Press.
Baker S, Hall R, Forde E. 1994. Geology and jungle fieldwork in eastern Indonesia. Geology T o d q 10:
18-23.
Boero F, BouillonJ. 1993. Zoogeography and life cycle patterns of Mediterranean hydromedusae (Cnidaria).
BiologicalJoumal o f h e Linnean So&& 48: 239-266.
Bremer K. 1992. Ancestral areas: a cladistic reinterpretation of the centre of origin concept. Systematit Biolagy 41:
436-445.
Brooks DR. 1990. Parsimony analysis in historical biogeography and coevolution: methodological and theoretical
update. $&matic <oology 39: 14-30.
Brooks DR, Thorson TB, Mayes MA. 1981. Freshwater stingrays (Potamotrygonidae)and their helminth
parasites. In: Funk VA, Brooh DR, eds. Advances in Cludirhcs. New York New York Botanical Garden.
Cracraft J. 1994. Species diversity, biogeography, and the evolution of biotas. American <oologif 34: 3 3 4 7 .
Hamilton WB. 1988. Plate tectonics and island arcs. Geological So&& ofAmerica Bulktin 100: 1503-1527.
Hilrlin M, Sundberg P. 1995. Cladistic analysis of the eureptantic nemerteans (Nemertea, Hoplonemertea).
Inwtebrate Tuonomy 9: 121 1-1229.
Harold AS, Mooi RD. 1994. Areas of endemism: definition and recognition criteria. Systematic Biology 43:
26 I --266.
Hillis DM, HuelsenbeckJP. 1992. Signal, noise, and reliability in molecular phylogenetic analyses. Journal of
Hmedib 83: 18% 195.
Humphries CJ, Parenti LR. 1986. Chititic biogcogrphy. Oxford: Clarendon Press.
Kirkpatrick M, Slatkin M. 1993. Searching for evolutionary patterns in the shape of a phylogenetic tree.
Evoluhn47: 1171-1181.
Klassen GJ, Mooi RD, Locke A. 1991. Consistency indices and random data. syslematic <oology 40: 4 4 W 5 7 .
Kluge AG. 1988. Parsimony in vicariance biogeography: a quantitative method and a greater Andean example.
$~tem~tic<oo~@ 37: 3 15-328.
Maddison DR, Ruolvo M, Swofford DL. 1992. Geographic origin of human mitochondrial DNA
phylogenetic evidence from control region sequences. Syslematic Biology 41: 1 1 1-124.
Maddison WP, Maddison DR. 1992. MacClade: Anah& of phylogeny and charach euolution. Version 3.0.
Sunderland, Massachusetts: Sinauer Associates.
Mishler BD, Donoghue IyI. 1982. Species concepts: a case of pluralism. Syslematic <oology 31: 491-503.
MorroneJJ, CarpenterJM. 1994. In search of a method for cladistic biogeography: an empirical comparison
of competent analysis, Brooks parsimony analysis, and three-area statements. Chiirtics 10: 99-1 53.
Nelson G, Ladiges PY. 1991. Three-area statements: standard assumptions for biogeographic analysis. $stmutit
<OO~OQ
40: 470-485.
Nelson G, Platnick NI. 1981. syslemahcs and biogeography. Chititits and Vicariance. New York: Columbia University
Press.
Page RDM. 1988. Quantitative cladistic biogeography: constructing and comparing area cladograms. +!matic
zoo lo^ 37: 254-270.
Page RbM. 1990. Component analysis: a valiant failure? Chititics 6: 119-136.
342
M. I-L&LIN
Page RDM. 1993. COMPO"i7 Version 2.0. Computer program published by the author. London: The Natural
History Museum.
Page RDM. 1994. Maps between trees and cladistic analysis of historical associations among genes, organisms, and
areas. Sysrcmatic BWlOgv 431 58-77.
Parenti LR. 1991. Ocean basins and the biogeography of freshwater fishes. Australian SystemariC Botany 41
137-1 49.
Ronquist F. 1994. Ancestral areas and parsimony. Systematic Bwlogv 431 267-274.
Sober E. 1988. The conceptual relationship of cladistic phylogenetics and vicariance biogeography. systematic
<OOI&
37: 245-253.
Sdasny-WijnhoffG. 1925. On a collection of numerteans from Curacao. Bidrqgm tot & K i n i s drr Fauna van Curacao
24: 97-120.
Stiaany-Wijnhoff G. 1926. The Nemertea Polystilfera of Naples. fibblicazioni delh S&wne <oologia di Napoli 7:
11S168.
Sundberg P, Svensaon M. 1994. Homoplasy, character function and nemertean systematics.Journal cf<oology,
London 234: 253-263.
Swofford DL. 1993. PAUP: Phyrogrnctic anabsis uringparsimony. Version 3. I . 1. Computer program distributed by the
Illinois Natural History Survey, Champaign, Illinois.
Wallace CC, PandolfiJM, Youug A, Woletenholme J. 1991. Indo-Pacific coral biogeography: a case study
from the Acropora selago group. Australian $ystnnatic Bohy 41 199-210.
Wiley EO. 1988. Parsimony analysis and vicariance biogeography. Systnnatic <oology 371 271-290.
Winterbottom R, McLenaan DA 1993. Cladogram versatility: evolution and biogeography of acanthuroid
fishes. Evolution 47: 1557-1 57 I .