Blackwell Publishing LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2006?

2006
88?
193202
Original Article

COLOUR CHARACTERS IN PHYLOGENETIC RECONSTRUCTION

B. AREEKUL and D. L. J. QUICKE

Biological Journal of the Linnean Society, 2006, 88, 193–202. With 2 figures

The use of colour characters in phylogenetic

reconstruction
BUNTIKA AREEKUL1† and DONALD L. J. QUICKE1,2*
1
Division of Biology, and Centre for Population Biology, Imperial College London, Silwood Park Campus,
Ascot, Berkshire SL5 7PY, UK
2
Department of Entomology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK

Received 8 November 2004; accepted for publication 25 July 2005

The use of coloration as a source of characters in phylogenetic reconstruction is investigated using 54 published data
sets. Studies were divided into two categories based on a priori postulated roles of the coloration: (1) aposematic and
mimetic coloration and (2) nonaposematic, nonmimetic coloration plus dual signals. Colour characters superficially
appear to provide similar phylogenetic signal to morphological ones in the case of aposematic and mimetic coloration
but significantly less in other situations. However, the data indicated that the apparent signal in the aposematic/
mimetic studies tends to be in greater conflict with the morphological signal. It is proposed that this reflects con-
straints in the evolution of colour characters that are part of aposematic/mimetic patterns and not that they are nec-
essarily good indicators of phylogeny. © 2006 The Linnean Society of London, Biological Journal of the Linnean
Society, 2006, 88, 193–202.

ADDITIONAL KEYWORDS: aposematism – coloration – crypsis – ILD – mimicry – phylogenetic signal.

INTRODUCTION have been used (e.g. nudibranch molluscs; Gosliner &

Johnson, 1999) they have resulted in greater phyloge-
Colour pattern features are involved in many inter- netic resolution, perhaps suggesting that colour char-
and intraspecific interactions, including species and acters should be used more in phylogeny. Surprisingly,
sexual recognition, mimicry, warning signals, and in two recent species-level phylogenetic studies of par-
camouflage. Colour characters are often employed in asitic wasps, Braet & Quicke (2003) on Stantonia Ash-
species identification and, although colour may vary mead (Braconidae, Orgilinae) and Areekul & Quicke,
intraspecifically due to environmental, ontogenetic, 2006) on Yelicones Cameron (Braconidae, Rogadinae)
and dietary factors, as well as genetic variation (Wiley, in which numerous colour characters were scored for
1981; Quicke, 1993; Winston, 1999), or fade in the phylogenetic analyses, coloration was found to per-
museum specimens, elements of colour patterns can form better than morphology in terms of how well
nevertheless provide reliable features for species iden- colour characters fitted on to the most parsimonious
tification. Indeed, in some groups of organisms, spe- tree (MPT) obtained from simultaneous analysis of all
cies level taxonomy has relied heavily on colour characters. Initially, these results suggest that color-
characters because of their relative morphological ation may provide at least as much phylogenetic sig-
homogeneity and the lack of fresh material for molec- nal as does morphology, if not more. However, we
ular or other studies. However, the utility of colour fea- predict that colour features included in aposematic,
tures for phylogenetic reconstruction has not been Batesian, and Müllerian mimicry patterns will not
rigorously investigated, and they appear to have been evolve according to the same rules as morphological
deliberately excluded by many workers because of characters or nonaposematic colour characters. Thus,
worries over their plasticity. In some cases where they colour pattern elements may not be as free to evolve
independently of one another, selection acting to main-
tain a successful pattern (Quicke, 1992). By contrast,
*Corresponding author. E-mail: d.quicke@imperial.ac.uk
†Current address: Department of Biology, Faculty of Science, we suggest that morphological characters will in gen-
Chulalongkorn University, Bangkok, Thailand. eral be more free to evolve independently of one

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202 193
194 B. AREEKUL and D. L. J. QUICKE
another because, in most studies, they will be sampled
from numerous functionally different systems. If so,
then colour characters will not display the same level
of homoplasy as morphological characters on MPT to
which they contribute (Braet & Quicke, 2003).
MATERIAL AND METHODS
CONSTRUCTION OF MOST PARSIMONIOUS TREES AND
CHARACTER FIT
Fifty-four morphology-based phylogenies, including
between 3% to 66% of colour characters, for which
original data sets were available either in the litera-
ture (from the internet or directly from the authors)
were assembled to investigate the behaviour of color-
ation in phylogenetic reconstruction (Table 1). We
divided the data sets a priori into two categories based
on the nature of their colour characters: (1) apose-
matic and/or mimetic coloration (termed A/M) and
(2) nonaposematic, nonmimetic coloration (e.g. cryptic
coloration, sexual, and species recognition) plus
ambiguous dual signals (termed NA/NM) (Table 1).
The data sets were then reanalysed with all charac-
ters treated (i.e. ordering and weighting) as in their
respective original studies. Heuristic tree searches
were carried out on the whole data sets (i.e. simul-
taneous analysis of colour and morphological
(noncolour) characters) using PAUP* (version 4.0b10)
(Swofford, 1998). Each search comprised 1000 random
additions, followed by tree bisection reconnection
branch swapping on a maximum of one tree
(NCHUCK = 1 CHUCKSCORE = 1). Although this
strategy will not generally find most parsimonious
trees with large data sets, it enables a lot of tree space
to be explored in a reasonable time, and the trees
found are generally likely to be fairly similar to the
MPTs. The morphological and colour character parti-
tions were then mapped separately on to the MPT(s)
from the simultaneous analysis of the whole data set,
and the ensemble retention indices (RIs) were then
calculated for each partition.
DETERMINING RELATIVE SIGNAL STRENGTH OF
PARTITIONS
The second important consideration is whether one
data partition carries more apparent signal than the
other. Thus, data constituting one partition may fit
poorly on to the MPT from simultaneous analysis of
both partitions either due to real conflict in the trees
they support or because one data set simply contains
more noise, and therefore the other will be dominant
in the combined analysis. Dominance of one data par-
tition over the other could be due either to the number
of characters in the partition or to the strength of the
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
apparent phylogenetic signal per character. The poten-
tial dominance of one partition over the other was
tested by assigning different weights to each partition
in an additional series of combined analyses (differen-
tial weighting) and then comparing the resultant tree
with those from equally weighted analysis. Similari-
ties between these trees were assessed using the
agreement subtrees (AST) option implemented in
PAUP* (version 4.0b10) (Swofford, 1998). If MPTs cal-
culated from each weighted analysis resulted in more
than ten trees, ten randomly selected MPTs were com-
pared with the MPT(s) from the equally weighted
analysis (Østergaard, Boxshall and Quicke, 2003).
In total, 12 weighted analyses were performed
for each data set, with morphological characters
upweighted 1.25, 1.5, 2, 5, 10, and 1000 relative to
colour ones and vice versa. Although none of the data
sets had anywhere near 1000 characters, a weighting
of 1000 : 1 was used instead of infinity to overcome the
possibility that trees will become much more unre-
solved when one partition is assigned zero weight
(because fewer characters are available to provide res-
olution), which would cause a misleading reduction in
the number of taxa retained in the AST. This is espe-
cially likely to be problematic when morphological
characters are weighted zero because the remaining
colour characters on average comprised a smaller pro-
portion of the total character set.
If the two partitions provide equally strong but
conflicting signals, then the MPTs from an equally
weighted analysis are likely to represent, at best, a
compromise, and giving either partition greater and
greater weight will lead to trees that tend more to
reflect the signal in that partition and, consequently,
the proportion of taxa retained in the ASTs from the
MPTs from such differentially weighted analyses and
an equally weighted one will decline rapidly with the
degree of differential weighting. In the case of two par-
titions providing equally strong apparent phylogenetic
signal, on average, a plot of the proportion of taxa
retained in the AST(s) (from differentially weighted
and equally weighted MPTs) vs. up-weighting factor
will be symmetric.
The degree of asymmetry in the proportion of taxa
retained in ASTs with upweighting colour vs. nonco-
lour characters (or vice versa) is a measure of the
degree of real conflict between the apparent phyloge-
netic signals originating from the two character
partitions as opposed to conflict due to differential
amounts of noise (Dolphin et al., 2000). By contrast to
Østergaard et al. (2003), when two partitions support
different phylogenetic hypotheses and one is dominant
to the other (i.e. it carries stronger apparent phyloge-
netic signal), upweighting the dominant partition will
not reduce (or will reduce relatively less) the number
of taxa retained in the AST(s) (from the differentially
 Table 1. Classification, source and retention indices (RI) for colour and morphological characters. Studies in which colour characters have a larger RI than
morphological one are indicated in bold

No. of No. of Ratio colour

Ref. noncolour colour RI RI RI/morphology
Organisms A/M Data source abbr. characters characters morphology colour RI Comments

Cidaria Treitschke (Lepidoptera: No Choi (1998) a 24 6 0.737 0.778 1.056 Cryptic

Geometridae)
Leucopine spp. (Diptera: No Gaimari & b 15 3 0.875 0.889 1.016 Cryptic
Chamaemyiidae) Tanasijtshuk (2001)
Urosaurus spp. (Reptilia: Squamata: No Wiens (1993) c 29 5 0.846 1.000 1.180 Cryptic
Phrynosomatidae)
Cnemidophorus spp. (Reptilia: No Grismer (1999) d 12 6 0.500 1.000 2.000 Cryptic
Squamata: Teiidae)
Oneida Hulst (Lepidoptera: Pyralidae) No Solis (1991) e 9 7 1.000 0.800 0.800 Cryptic
Juditha, Lemonias, Thisbe, Uraneis Yes Hall & Harvey (2001a) f 40 29 0.921 0.862 0.936 Mimicry
spp. (Lepidoptera: Riodinidae)
Cacophis spp. (Serpentes: Elapidae) No Scandon (2003) g 13 6 0.500 0.500 1.000 Cryptic
Nerthra alaticollis (Heteroptera: No Cassis & Silveira h 18 2 0.765 1.000 1.307 Cryptic
Gelastocoridae) (2001)
Anopheles spp. (Diptera: Culicidae) No Anthony, Harbach & i 19 5 0.586 0.500 0.853 Cryptic
Kitching (1997)
Charis cleonus complex (Lepidoptera: No Harvey & Hall (2002) j 32 4 0.875 0.885 1.011 Mixed,
Riodinidae) cryptic/
aposematic
Hepialid moths (Lepidoptera: No Brown et al. (2000) k 60 3 0.820 0.667 0.813 Cryptic
Hepialidae)
Polygonia, Nymphalis spp. No Nylin et al. (2001) l 46 51 0.731 0.726 0.993 Mixed signal
(Lepidoptera: Nymphalidae)
Characidiin fish (Characiformes: No Buckup (1993) m 48 16 0.748 0.894 1.195 Cryptic
Ostariophysi)
Rheumatobates spp. (Heteroptera: No Westlake, Rowe & n 98 4 0.846 0.732 0.865 Cryptic
Gerridae) Currie (2000)

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
Bonjeanis Irwin & Lyneborg (Diptera: No Winterton et al. o 43 13 0.779 0.554 0.711 Cryptic
Therevidae) (2000)
Chelinini (Pisces: Labridae) No Westneat (1993) p 68 18 0.901 0.832 0.923 Sexual
recognition
Phalangogonia Burmeister No Smith & Morón (2003) q 30 2 0.721 0.400 0.555 Sexual
(Coleoptera: Scarabaeidae) recognition
COLOUR CHARACTERS IN PHYLOGENETIC RECONSTRUCTION

Charis and Calephelis (Lepidoptera: No Hall & Harvey (2002b) r 13 18 0.833 0.746 0.896 Cryptic/
Riodinidae) sexual
recognition
195

A/M, Aposematic or mimetic coloration.

 Table 1. Continued
196

No. of No. of Ratio colour

Ref. noncolour colour RI RI RI/morphology
Organisms A/M Data source abbr. characters characters morphology colour RI Comments

Coladenia Moore (Lepidoptera: No De Jong (1996) s 14 9 0.862 0.735 0.853 Dual signals
Hesperiidae)
Cryptodacus, Haywardina and No Norrbom (1994) t 26 24 0.863 0.754 0.874 Cryptic
Rhagoletotrypeta (Diptera:
Tephritidae)
Ceratitis spp. (Diptera: Tephritidae) No Meyer (2002) u 14 16 0.938 0.375 0.400 Sexual
recognition
Pandivirilia spp. (Diptera: Therevidae) No Webb & Metz (2003) v 28 2 0.794 0.500 0.630 Cryptic/
sexual
recognition
B. AREEKUL and D. L. J. QUICKE

Hypselodoris spp. (Nudibranchia: No Gosliner & Johnson w 46 13 0.676 0.738 1.092 Cryptic/
Chromodorididae) (1999) aposematic
Prosciara Frey (Diptera: Sciaridae) No Vilkamaa (2000) x 62 2 0.685 0.577 0.842 Cryptic
Gulls (Aves: Larinae) No Chu (1998) y 131 50 0.691 0.677 0.980 Cryptic
Fideliini (Hymenoptera: Megachilidae) No Engel (2002) z 26 2 0.926 0.500 0.540 Sexual
recognition
Therini (Lepidoptera: Geometridae) No Choi, (2000) aa 38 11 0.709 0.513 0.724 Cryptic/
sexual
recognition
Rionid butterflies (Lepidoptera: No Hall (2002) ab 75 29 0.867 0.815 0.940 Cryptic
Riodinidae)
Phrynosomatid lizard (Reptilia: No Reeder & Wiens ac 142 15 0.675 0.608 0.900 Cryptic/
Squamata: Phrynosomatidae) (1996) sexual
recognition
Elachistidae spp. (Lepidoptera: No Kaila (1999) ad 120 10 0.769 0.578 0.752 Cryptic
Gelechioidea)
Finches (Aves: Fringillidae) No Chu (2002) ae 172 53 0.534 0.407 0.762 Sexual
recognition
Sitobion Mordvilko (Hemiptera: No Jensen (1997) af 29 19 0.688 0.650 0.945 Cryptic
Aphididae)
Enallagma spp. (Odonata: Zygoptera) No May (2002) ag 30 18 0.752 0.564 0.750 Sexual
recognition
Agapostemon spp. (Hymenoptera: No Janjic & Pecker ah 127 23 0.513 0.479 0.934 Cryptic/
Halictidae) (2003) sexual
recognition
Homalolinus and Ehomalolinus spp. No Márquez (2003) ai 52 5 0.788 0.493 0.626 Cryptic
(Coleoptera: Staphylinidae)

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
A/M, Aposematic or mimetic coloration.
 No. of No. of Ratio colour
Ref. noncolour colour RI RI RI/morphology
Organisms A/M Data source abbr. characters characters morphology colour RI Comments

Flycatchers (Aves: Tyrannodae) No Birdsley (2002) aj 58 10 0.732 0.534 0.730 Sexual

recognition
Hypanartia spp. (Lepidoptera: Yes Willmott et al. (2001) ak 23 30 0.789 0.841 1.066 Mimicry
Nymphalidae)
Ariconis spp. (Lepidoptera: Riodinidae) Yes Hall & Harvey (2002a) al 18 9 0.969 1.000 1.032 Mimicry
Heliconiinae genera (Lepidoptera: Yes Penz & Peggie (2003) am 179 6 0.687 0.417 0.607 Mimicry
Nymphalidae)
Synargis spp. (Lepidoptera: Riodinidae) Yes Hall & Harvey (2002b) an 31 22 0.903 0.772 0.855 Mimicry/
aposematic
Charis gynea group (Lepidoptera: No Hall & Harvey (2001b) ao 9 8 0.824 0.824 1.000 Cryptic/
Riodiniidae) sexual
recognition
Josiini moths (Lepidoptera: Dioptinae) Yes Miller (1996) ap 71 15 0.848 0.812 0.958 Aposematic
Passion-vine butterflies (Lepidoptera: Yes Penz (1999) aq 136 10 0.828 0.816 0.986 Mimicry/
Nymphalidae) Aposematic
Enoclerus spp. (Coleoptera: Cleridae) Yes Mawdsley (2001a) ar 17 18 0.719 0.685 0.953 Mimicry
Acherontia Laspeyres (Lepidoptera: Yes Kitching, (2003) as 53 12 0.806 0.794 0.985 Mimicry
Sphingidae)
Aulicus Spinola (Coleoptera: Cleridae) Yes Mawdsley (2001b) at 11 6 0.414 0.846 2.043 Mimicry
Morpho butterflies (Lepidoptera: Yes Penz & DeVries au 89 31 0.598 0.558 0.933 Aposematic
Nymphalidae) (2002)
Eterusia (Lepidoptera: Zygaenidae) Yes Yen et al. (2005) av 31 49 0.988 0.813 0.823 Mimicry
Adelpha spp. (Lepidoptera: Yes Willmott (2003) aw 39 75 0.534 0.609 1.140 Mimicry
Nymphalidae)
Bonesioides spp. (Coleoptera: Yes Freund & Wagner ax 29 5 0.684 0.475 0.694 Mimcry
Chrysomelidae) (2003)
Stantonia spp. (Hymenoptera: Yes Braet & Quicke (2003) ay 81 24 0.609 0.655 1.078 Aposematic
Braconidae)
Eulithis Hübner (Lepidoptera: Yes Choi (2001) az 40 11 0.402 0.328 0.816 Mimicry
Geometridae)

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
Alabagrus spp. (Hymenoptera: Yes Sharkey (1988) ba 35 20 0.813 0.761 0.936 Aposematic
Braconidae)
Yelicones spp. (Hymenoptera: Yes Areekul & Quicke bb 57 29 0.497 0.540 1.087 Aposematic
Braconidae) (2006)

A/M, Aposematic or mimetic coloration.

COLOUR CHARACTERS IN PHYLOGENETIC RECONSTRUCTION
197
198 B. AREEKUL and D. L. J. QUICKE

weighted and equally weighted analyses) compared
with upweighting the other partition. This is because,
in the latter case, even when a small or moderately
higher weight is given to the other (nondominant) par-
tition, the nonupweighted (dominant) partition is still
able to have an influence on the tree.
Asymmetry in plots of the proportion of taxa
retained in ASTs in each category was assessed using
the Wilcoxon matched pairs test to compare the mor-
phological upweighted proportions of retained taxa
with those from equivalently upweighted colour char-
acters. The proportion of taxa in ASTs with different
weights were compared between A/M and NA/NM cat-
egories using Mann–Whitney U-tests.
RESULTS AND DISCUSSION
The proportion of colour characters in A/M and NA/
NM data sets was not significantly different (t = 1.53,
d.f. = 30, P = 0.136) and therefore revealed differences
in the apparent phylogenetic signal strength are
likely to be intrinsic to the type of data rather than
the relative numbers of characters. Fourteen of the
54 phylogenies (26%) have the RI of colour characters
higher than morphological ones (Table 1) suggesting
that, in a substantial number of cases, coloration may
provide a valuable source of phylogenetic signal.
Seven of the cases in which coloration had a higher
RI were in the A/M category, a significantly higher
proportion than in the NA/NM category (χ2 = 4.12,
d.f. = 1, P < 0.5) which would appear to suggest that,
in A/M cases, coloration is potentially a good indica-
tor of phylogeny whereas, in NA/NM cases, it was
more homoplastic. However, differential weighting of
colour and morphological characters in the NA/NM
category showed a marked degree of asymmetry in
the proportion of taxa retained in the ASTs with mor-
phological characters generally providing a stronger
signal (Fig. 1). This asymmetry was significant
with relative partition weights of 5 : 1 and higher
(Table 2), again indicating that the colour characters
provide a weaker phylogenetic signal. However, in A/
M cases, the asymmetry was far less marked and the
difference between upweighting colour and upweight-
ing morphology was only significant with the most
extreme weighting (1000 : 1) (Fig. 2, Table 2). How-
ever, comparison of Figures 1 and 2 shows that the
lower asymmetry in the case of A/M studies is not
due to the effect of upweighting colour characters
being less, but that upweighting morphology (left side
of graph) led to a more marked reduction in the pro-
portion of taxa in the ASTs. Comparison of A/M and

120
Non-aposematic/ non-mimetic coloration (NA/NM)
a,b,c,d,e,f,g, h
i
j
100 k
l
m,n
o
p
80 q
r
median
s
t
60 u, v
w
x
y
z
40 aa
ab
ac
ad
ae
20 af
ag
ah

0
0.001 0.1 0.2 0.5 0.67 0.8 1 1.25 1.5 2 5 10 1000
Relative weighting of colour character partition

Figure 1. Percentage of taxa retained in agreement subtrees from equally and differentially weighted analyses for
NA/NM studies. The median values are indicated in black; letters refer to published data sources (Table 1).

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
 COLOUR CHARACTERS IN PHYLOGENETIC RECONSTRUCTION 199

120
Aposematic/ mimetic coloration (A/M)

100

ak
al
am
80 an
ao
ap
aq
ar
60 median
as
at
au
av
40 aw
ax
ay
az
ba
20

0
0.001 0.1 0.2 0.5 0.67 0.8 1 1.25 1.5 2 5 10 1000
Relative weighting of colour character partition

Figure 2. Percentage of taxa retained in agreement subtrees from equally and differentially weighted analyses for A/M
studies. The median values are indicated in black; letters refer to published data sources (Table 1).

Table 2. Comparisons of the proportions of taxa retained Table 3. Comparison of proportions of taxa retained in
in agreement subtrees with different weighting of morpho- agreement subtrees between NA/NM and A/M studies at
logical vs. colour characters within NA/NM and A/M cate- each relative weighting level (Mann–Whitney U-test)
gories (Wilcoxon test)
Weight P-values
P-values
Morphological characters
Weights NA/NM + dual signals A/M 1000 0.0099*
10 0.0136*
1.25 0.8720 0.2941 5 0.0104*
1.5 0.3754 0.1956 2 0.0359*
2 0.0612 0.3378 1.5 0.0885
5 0.0095* 0.1834 1.25 0.1335
10 0.0011* 0.0921 Colour characters
1000 0.0002* 0.0276* 1.25 0.0548
1.5 0.1446
*Significant P values (P < 0.05). 2 0.0951
5 0.0838
NA/NM studies showed that this became significant
10 0.1635
when morphology was upweighted by a factor of two 1000 0.2420
(Table 3). This pattern indicates that there is greater
conflict between the morphological and colour parti- *Significant P values (P < 0.05).
tions in the A/M cases. Although theoretically incon-
gruence length difference tests (Farris et al., 1994) between the incongruence in each case (Dolphin
could be used to investigate this, the analyses would et al., 2000).
be impracticable because of the very large number of The above results indicate that the way colour char-
replicates that would be required to differentiate acters behave in phylogenetic reconstruction varies

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
200 B. AREEKUL and D. L. J. QUICKE
according to the biological role of the colour pattern.
The direction of the difference is in agreement with
our prior expectation that colour characters involved
in strongly conserved patterns, such as in Müllerian
and Batesian mimicry or particular cases of aposema-
tism, cannot evolve as independently from one
another as many morphological ones might because
changes in any element of such colour patterns are
likely to reduce the mimetic relationships. This will
have two consequences: (1) colour characters involved
in A/M studies may be more phylogenetically con-
strained and (2) because they are directly related to
the colour pattern as a whole, they may show strongly
structured evolution possibly giving rise to an appar-
ently strong phylogenetic signal that is in conflict with
the morphological signal. Thus, we caution against
including colour characters from A/M patterns in phy-
logenetic reconstruction.
ACKNOWLEDGEMENTS
We would like to thank P. C. Chu, J. P. W. Hall, M. S.
Engel, and L. Packer for providing us with their data
sets and comments on the biological role of colour. We
thank Andy Purvis, David Orme, Pia Østergaard, and
Shen-Horn Yen for helpful discussion.
REFERENCES
Anthony TG, Harbach RE, Kitching IJ. 1999. Phylogeny
of the Pyretophorus series of Anopheles subgenus Cellia
(Diptera: Culicidae). Systematic Entomology 24: 193–205.
Areekul B, Quicke DLJ. 2006. Systematics of the parasitic
wasp genus Yelicones Cameron (Hymenoptera: Braconidae:
Rogadinae) and revision of the genus from North, Central and
South America. Systematics and Biodiversity, in press.
Birdsley JS. 2002. Phylogeny of the tyrant flycatchers
(Tyrannidae) based on morphology and behavior. Auk 119:
715–734.
Braet Y, Quicke DLJ. 2004. A phylogenetic analysis of the
Mimagathidini with revisionary notes on the genus Stanto-
nia Ashmead, 1904 (Hymenoptera: Braconidae: Orgilinae).
Journal of Natural History 38: 1489–1589.
Brown B, Dugdale JS, Emberson RM, Paterson AM. 2000.
Phylogeny of New Zealand hepialid moths (Lepidoptera:
Hepialidae) inferred from a cladistic analysis of morpholog-
ical data. Systematic Entomology 25: 1–14.
Buckup PA. 1993. Phylogenetic interrelationships and reduc-
tive evolution in Neotropical characidiin fishes (Characi-
formes, Ostariophysi). Cladistics 9: 305–341.
Cassis G, Silveira R. 2001. A revision and phylogenetic anal-
ysis of the Nerthra alaticollis species-group (Heteroptera:
Gelastocoridae: Nerthrinae). Journal of the New York Ento-
mological Society 109: 1–46.
Choi SW. 1998. Systematics of the genus Cidaria Treitschke
(Lepidoptera, Geometridae, Larentiinae). Zoological Journal
of the Linnean Society 122: 555–580.
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
Choi SW. 2000. A cladistic analysis of the Therini: a new syn-
onym of the Cidariini (Lepidoptera: Geometridae, Larentii-
nae). American Museum Novitiates 3295: 1–25.
Choi SW. 2001. Phylogeny of Eulithis Hübner and related
genera (Lepidoptera: Geometridae), with an implication of
wing pattern evolution. American Museum Novitiates 3318:
1–24.
Chu PC. 1998. A phylogeny of the gulls (Aves: Larinae)
inferred from osteological and integumentary characters.
Cladistics 14: 1–43.
Chu PC. 2002. A morphological test of the monophyly of the
cardueline finches (Aves: Fringillidae, Carduelinae). Cladis-
tics 18: 279–312.
De Jong R. 1996. The continental Asian element in the fauna
of the Philippines as exemplified by Coladenia Moore, 1881
(Lepidoptera: Hesperiidae). Cladistics 12: 323–348.
Dolphin K, Belshaw R, Orme CDL, Quicke DLJ. 2000.
Noise and incongruence: interpreting results of the incongru-
ence length difference test. Molecular Phylogenetics and
Evolution 17: 401–406.
Engel MS. 2002. Phylogeny of the bee tribe Fideliini
(Hymenoptera: Megachilidae), with the description of a new
genus from southern Africa. African Entomology 10: 305–
313.
Farris JS, Kallersjo M, Kluge AG, Bult C. 1994. Testing sig-
nificance of incongruence. Cladistics 10: 315–319.
Freund W, Wagner TH. 2003. Revision of Bonesioides Labois-
sière, 1925 (Coleoptera; Chrysomelidae; Galerucinae) from
continental Africa. Journal of Natural History 37: 1915–
1976.
Gaimari SD, Tanasijtshuk V. 2001. A new leucopine genus
(Diptera: Chamaemyiidae) with species attacking Ceroplas-
tes wax scales (Hemiptera: Coccidae) in South America. Sys-
tematic Entomology 26: 311–328.
Gosliner TM, Johnson RF. 1999. Phylogeny of Hypselodoris
(Nudibranchia: Chromodorididae) with a review of the mono-
phyletic clade of Indo-Pacific species, including descriptions
of twelve new species. Zoological Journal of the Linnean
Society 125: 1–114.
Grismer LL. 1999. Phylogeny, taxonomy, and biogeography of
Cnemidophorus hyperythrus and C. ceralbensis (Squamata:
Teiidae) in Baja California, México. Herpetologica 55: 28–42.
Hall JPW. 2002. Phylogeny of the riodinid butterfly tribe
Theopeina (Lepidoptera: Riodinidae: Nymphidini). System-
atic Entomology 27: 139–167.
Hall JPW, Harvey DJ. 2001a. A phylogenetic analysis of the
Neotropical riodinid butterfly genera Juditha, Lemonias,
Thisbe and Uraneis, with a revision of Juditha (Lepidoptera:
Riodinidae: Nymphidiini). Systematic Entomology 26: 453–
490.
Hall JPW, Harvey DJ. 2001b. Phylogenetic revision of the
Charis gynaes group (Lepidoptera: Riodinidae) with com-
ments on historical relationships among Neotropical areas of
endemism. Annals of the Entomological Society of America
94: 631–647.
Hall JPW, Harvey DJ. 2002a. A phylogenetic review of
Charis and Calephelis (Lepidoptera: Riodinidae). Annals of
the Entomological Society of America 95: 407–421.
 COLOUR CHARACTERS IN PHYLOGENETIC RECONSTRUCTION
Hall JPW, Harvey DJ. 2002b. Basal subtribes of the
Nymphidiini (Lepidoptera: Riodinidae): phylogeny and
myrmecophily. Cladistics 18: 539–569.
Harvey DJ, Hall JPW. 2002. Phylogenetic revision of the
Charis cleonus complex (Lepidoptera: Riodinidae). System-
atic Entomology 27: 265–300.
Janjic J, Packer L. 2003. Phylogeny of the bee genus Aga-
postemon (Hymenoptera: Halicitidae). Systematic Entomol-
ogy 28: 101–123.
Jensen AS. 1997. Redefinition of the aphid genus Sitobion
Mordvilko (Hemiptera: Aphididae) based on cladistic analy-
ses, with emphasis on North American species. Systematic
Entomology 22: 333–344.
Kaila L. 1999. Phylogeny and classification of the Elachistidae
s.s. (Lepidoptera: Gelechioidea). Systematic Entomology 24:
139–169.
Kitching IJ. 2003. Phylogeny of the death’s head hawkmoths,
Acherontia [Laspeyres], and related genera (Lepidoptera:
Sphingidae: Sphinginae: Acherontiini). Systematic Entomol-
ogy 28: 71–88.
Márquez J. 2003. Systematic revision of the genera Homaloli-
nus and Ehomalolinus (Coleoptera, Staphylinidae, Xantho-
linini). Zoologica Scripta 32: 491–523.
Mawdsley JR. 2001a. Cladistic analysis of Nearctic species of
Enoclerus Gaham with discussion of evolution of mimicry
and cryptic coloration. Transactions of the American Ento-
mological Society 127: 459–471,.
Mawdsley JR. 2001b. Cladistic analysis of the Nearctic
checkered beetle genus Aulicus Spinola (Coleoptera:
Cleridae: Clerinae). Journal of the New York Entomological
Society 109: 337–343.
May ML. 2002. Phylogeny and taxonomy of the damselfly
genus Enallagma and related taxa (Odonata: Zygoptera:
Coenagrionidae). Systematic Entomology 27: 387–408.
Meyer M. 2000. Systematic revision of the subgenus Ceratitis
Macleay s.s. (Diptera, Tephritidae). Zoological Journal of the
Linnean Society 127: 459–471.
Miller JS. 1996. Phylogeny of the Neotropical moth tribe Josi-
ini (Notodontidae: Dioptinae): a hidden case of Müllerian
mimicry. Zoological Journal of the Linnean Society 118: 1–
45.
Norrbom AL. 1994. New species and phylogenetic analysis of
Cryptodacus, Haywardina and Rhagoletotrypeta (Diptera:
Tephritidae). Insecta Mundi 8: 37–65.
Nylin S, Nyblom K, Ronquist F, Janz N, Belicek J,
Källersjö M. 2001. Phylogeny of Polygonia, Nymphalis and
related butterflies (lepidoptera: Nymphalidae): a total evi-
dence analysis. Zoological Journal of the Linnean Society
132: 441–468.
Østergaard P, Boxshall GA, Quicke DLJ. 2003. Phylogeny
within the Chondracanthidae (Poecilostomatoida, Copep-
oda). Zoologica Scripta 32: 299–319.
Penz CM. 1999. Higher level phylogeny for the passion-vine
butterflies (nymphalidae, Heliconiinae) based on early stage
and adult morphology. Zoological Journal of the Linnean
Society 127: 277–344.
Penz CM, DeVries PJ. 2002. Phylogenetic analysis of Morpho
butterflies (Nymphalidae, Morphinae): implications for clas-
© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202
201
sification and natural history. American Museum Novitates
3374: 1–33.
Penz CM, Peggie D. 2003. Phylogenetic relationships among
Heliconiinae genera based on morphology (Lepidoptera:
Nymphalidae). Systematic Entomology 28: 451–479.
Quicke DLJ. 1992. Batesian and Müllerian mimicry between
species with connected life histories, with a new example
involving braconid wasp parasites of Phoracantha beetles.
Journal of Natural History 26: 1013–1034.
Quicke DLJ. 1993. Principles and techniques of contemporary
taxonomy. Glasgow: Blackie Publishing Group.
Reeder TW, Wiens JJ. 1996. Evolution of the lizard family
Phrynosomatidae as inferred from diverse types of data. Her-
petological Monographs 10: 43–84.
Scandon JD. 2003. The Australian elapid genus Cacophis:
morphology and phylogeny of rainforest crowned snakes.
Herpetological Journal 13: 1–20.
Sharkey MJ. 1988. A taxonomic revision of Alabagrus
(Hymenoptera: Braconidae). Bulletin of the British Museum
(Natural History) 57: 311–437.
Smith ABT, Morón MA. 2003. Revision and phylo-
genetic analysis of the Central American endemic genus
Phalangogonia Burmeister (Coleoptera: Scarabaeidae:
Rutelinae: Anoplognathini). Systematic Entomology 28: 323–
338.
Solis MA. 1991. Revision and phylogenetic analysis of the
New World genus Oneida Hulst (Lepidoptera: Pyralidae:
Epipaschiinae), description of a new genus and comments on
the coding of scale color characters. Proceedings of the Ento-
mological Society of Washington 93: 808–827.
Swofford DL. 1998. PAUP*. Phylogenetic analysis using par-
simony (* and other methods), Version 4. Sunderland, MA:
Sinaeuer.
Vilkamaa P. 2000. Phylogeny of Prosciara Frey and related
genera (Diptera: Sciaridae). Systematic Entomology 25: 47–
72.
Webb DW, Metz MA. 2003. The Nearctic species of Pandivi-
rilia Irwin and Lyneborg (Diptera: Therevidae: Therevinae).
Annals of the Entomological Society of America 96: 369–402.
Westlake KP, Rowe L, Currie DC. 2000. Phylogeny of the
water strider genus Rheumatobates (Heteroptera: Gerridae).
Systematic Entomology 25: 125–145.
Westneat MW. 1993. Phylogenetic relationships of the tribe
Cheilinini (Labridae: Perciformes). Bulletin of Marine Sci-
ence 52: 351–394.
Wiens JJ. 1993. Phylogenetic systematics of the tree lizards
(genus Urosaurus). Herpetologica 49: 399–420.
Wiley EO. 1981. Phylogenetics. The theory and practice of
phylogenetic systematics. New York, NY: John Wiley &
Sons.
Willmott KR. 2003. Cladistic analysis of the Neotropical
butterfly genus Adelpha (Lepidoptera: Nymphalidae), with
comments on the subtribal classification of Limenitidini.
Systematic Entomology 28: 279–322.
Willmott KR, Hall JPW, Lamas G. 2001. Systematics of
Hypanartia (Lepidoptera: Nymphalidae: Nymphalinae),
with a test for geographical speciation mechanisms in the
Andes. Systematic Entomology 26: 369–399.
202 B. AREEKUL and D. L. J. QUICKE

Winston JE. 1999. Describing species. Practical taxonomic
procedure for biologists. New York, NY: Columbia University
Press.
Winterton SL, Skevington JH, Irwin ME, Yeates DK.
2000. Phylogenetic revision of Bonjeania Irwin & Lyneborg
(Diptera: Therevidae). Systematic Entomology 25: 295–324.
Yen SH, Robinson GS, Quicke DLJ. 2005. Phylogeny, sys-
tematics and evolution of mimetic wing patterns of Eterusia
moths (Lepidoptera, Zygaenidae, Chalcosiini). Systematic
Entomology 30: 358–397.

© 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 88, 193–202