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Spatiotemporal variation in morphological evolution in the Oligocene–Recent

larger benthic foraminifera genus Cycloclypeus reveals geographically
undersampled speciation

Article  in  GeoResJ · March 2015

DOI: 10.1016/j.grj.2014.11.001

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 GeoResJ 5 (2015) 12–22

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journal homepage: www.elsevier.com/locate/GRJ

Spatiotemporal variation in morphological evolution in the

Oligocene–Recent larger benthic foraminifera genus Cycloclypeus reveals
geographically undersampled speciation
Willem Renema
Naturalis Biodiversity Center, PO Box 9517, 2300 RA Leiden, The Netherlands

a r t i c l e i n f o a b s t r a c t

Article history: Accurate assessment of location and timing of speciation of species is needed to discriminate between
Received 10 July 2014 macroevolutionary models explaining large scale biodiversity patterns. In this paper I evaluate fossil evi-
Revised 5 November 2014 dence of variation in geographical ranges through time, as well as spatio-temporal variation in morpho-
Accepted 7 November 2014
logical parameters to examine geographical aspects of speciation and range variation. Specifically I test
for geographical morphological stability within time slices and for temporal modes of morphological
change within lineages.
Keywords:
Past distribution ranges of all species of the large benthic foraminifera Cycloclypeus have been docu-
Morphological evolution
Speciation
mented on paleogeographic maps. From those samples with sufficiently well preserved specimens inter-
Large scale biodiversity patterns nal morphological data were measured and analysed.
Large benthic foraminifera Within a small sample of six species in a single genus of reef associated large benthic foraminifera evi-
dence for heterogeneity in geographic speciation modes, including vicariance, peripheral speciation, and
sympatric speciation in the centre of the range has been found. Morphological evolution was found to be
either homogeneous over large geographic ranges or spatially restricted. In time two gradually evolving
lineages were found. Furthermore, an evolutionary transition of two species that previously was regarded
as gradual, is shown to be punctuated with intermediate populations occurring restricted in both time
and space.
I demonstrate the marked heterogeneity of evolutionary processes and the difficulty to make assump-
tions regarding tempo and mode of evolution. Furthermore, I introduce the concept of geographically
undersampled punctuations. This example exposes some of the pitfalls when conclusions regarding
the mode and location of speciation are based on the combination of phylogeny and extant distribution
alone.
Ó 2014 Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/3.0/).

Introduction aspects and timing of speciation, extinction, and morphological

Coral reef organisms show markedly similar patterns of species
diversity, with a prominent hotspot in the Indo-Australian Archi-
pelago [42,14,26]. Conflicting hypotheses have highlighted the
importance of this area either as a centre of origin, overlap or accu-
mulation, with the presumed geographical locations of origins and
extinction of species the primary criterion for testing these hypoth-
eses (e.g., [23,5]). Geographical and temporal variation in species
richness is the result of overlapping individual species ranges.
The geographic range of species is determined by their location
of speciation, potentially followed by range expansion (and subse-
quent contractions and expansions) and finally by extinction [21].
Here I explore the fossil record to look for evidence of geographic
E-mail address: Willem.Renema@naturalis.nl
evolution and the implication of these data for the interpretation
of present day distribution patterns.
Commonly speciation modes are identified by the amount of
geographic separation of sister-species, usually grouped into allo-
patric, peripatric, parapatric and sympatric speciation (e.g., [15];
Fig. 1). Even though an overwhelming majority of extant species
are millions of years old [4,48], location of origination is often
inferred from distribution patterns and the phylogenetic relation-
ship of extant species (e.g., [41,8], but see also [4]). Especially in
long lived taxa with high dispersal capacity each of these specia-
tion modes can result in the same distribution pattern (Fig. 1).
Often it is assumed that geographic ranges are small at the time
of origination [55,21]. However, Bellwood and Meyer [4] argue that
vicariance events in species with large geographic ranges need not
result in a spatially restricted speciation event, and that especially

http://dx.doi.org/10.1016/j.grj.2014.11.001
2214-2428/Ó 2014 Published by Elsevier Ltd.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).
 W. Renema / GeoResJ 5 (2015) 12–22
in wide ranging marine taxa this might be an important speciation
mechanism. An example in the fossil record is provided in the
planktonic diatom genus Rhizosolenia, in which the morphological
separation of the ancestral Rhizosolenia bergonii and Rhizosolenia
praebergonii was observed over a 60° longitudinal equatorial tran-
sect [52,6]. Very few benthic organism have a sufficiently detailed
fossil record to allow the examination of these patterns in suffi-
cient detail to document the relative importance using empirical
data.
Large benthic foraminifera are known for their abundance and
diversity in the fossil record (e.g., [50,48]). Contrary to many other
widespread and abundant taxa which display morphological stasis
[36], in many larger benthic foraminifera a repeated, directional
morphological change has been inferred (e.g., [30]). Cycloclypeus
is the largest extant benthic foraminifera, and is represented by a
single extant species, Cycloclypeus carpenteri. The B-forms, derived
from sexual reproduction, can grow to 10 cm in diameter, but most
commonly do not grow beyond 5–6 cm diameter. The asexually
derived A-forms usually do not grow larger than 1 cm in diameter.
Cycloclypeus lives within the lower part of the photic zone [27,46].
Koba [33] found that its range encompassed those areas of the
South China Sea within the photic zone, with year round tempera-
tures at the sediment–water interface higher than 20 °C, and below
the storm wave-base.
The test of Cycloclypeus consists of a round initial chamber
(proloculus) followed by a partially embracing second chamber.
Fig. 1. Hypothetical range variation in the four most frequently used speciation models (from top to bottom: allopatric, parapetric, peripatric and sympatric) can result in
near identical present day geographic ranges of species. The fifth column shows how area-time plots of each modes would look like, the dashed lines represent the four steps
illustrated in columns 1–4.
13
These are followed by a series of undivided operculine chambers
and divided heterostegine chambers, before annular chambers
develop (Figs. 2 and 3). During evolution the proloculus tends to
increase in size, and the number of operculine and heterostegine
chambers decreases. The traditional interpretation of morphologi-
cal variation in Cycloclypeus is that they consist of a single morpho-
logical cline that evolved gradually over time and synchronously
over space [34,16,54]. Several studies noted problems in correla-
tion (e.g., [11,12]) between regions, or the presence of a second
lineage of Cycloclypeus in the Indonesian/Pacific Middle Miocene
(e.g., [54,34]).
This paper presents the spatio-temporal morphological evolu-
tion of an entire genus of large benthic foraminifera, Cycloclypeus
in an attempt to provide empirical data illustrating the above
mentioned hypothetical models. This study documents, for the
first time, morphological data that can be evaluated across both
the entire stratigraphical and geographical range of all species
in Cycloclypeus. This sheds new light on the morphological stabil-
ity of species throughout their geographic ranges, and the loca-
tion of speciation. Specifically, I will first illustrate variation in
their geographical range through time, secondly I will test the
hypothesis that during any given time interval there is only a sin-
gle species of Cycloclypeus present. If this hypothesis is rejected
geographic clustering of the multiple species will be assessed.
Finally, I will evaluate the morphological stability of lineages
through time.
14 W. Renema / GeoResJ 5 (2015) 12–22

distribution of these samples is less resolved. In total 139 samples

5 with the possible exception of East Africa and the northern Pacific.
4
27
1 tian are relatively poorly represented in the samples. Most occur-
2 rences in these stratigraphic bins are from thin sections of
18
11 3 surements from literature, the same morphological characters as
A chamberlets in the first annular chamber (Fig. 2) of the asexual,
Fig. 2. Internal morphology of Cycloclypeus with the measurements included in this
study indicated. Yellow: proloculus; green: deuteroloculus; light blue: operculine
chamber. Two heterostegine chambers are indicated by the numbers 4 and 5 in
black. The nepionic spire includes the proloculus, deuteroloculus, operculine, and
heterostegine chambers. Chambers 6 and more are annular chambers. In white the
number of chamberlets for the 4th, 5th, and 6th chamber are indicated. X: number
of precyclic chambers in the nepionic spire (in this case X = 5); sp4 5: number of
chamberlets in the 4th and 5th chambers (in this case sp4 5 = 29); Number of
chamberlets in first annular chamber (in this case = 27); the arrow indicates the
diameter of the proloculus. A indicates a stolon connecting two chamberlets in
successive chambers. In blue the canal system is shown. (For interpretation of the
references to colour in this figure legend, the reader is referred to the web version of
this article.)
Methods
Material
Exploitation of the fossil record for studies of geospatial varia-
tion in morphology is hampered by the data intensity and strati-
graphical resolution that is required. Sampling should be
adequately distributed throughout the entire geographic range in
each time interval, to confidently resolve variations in the extent
of past geographic ranges. For the distribution maps, the Oligocene
to Recent has been divided into ten time slices of 2–3 million years
duration each. Uneven duration of time slices cannot be avoided as
a result of stratigraphic resolution and available datum planes for
between regions correlation. The three time slices of longest dura-
tion are all when the distribution range was restricted (mostly) to
the Indo West Pacific ocean (IWP). In total >250 occurrences of
Cycloclypeus from well-illustrated literature sources and museum
collections form the basis for the temporal distribution maps.
Morphological variation in populations can only be measured
from isolated specimens, and the geographic and stratigraphic
containing over 4500 specimens have been included. Sampling is
relatively complete from most of the geographic range of the genus
in each time slice (Figs. 4 and 5; Supplementary material Table S1),
Indonesia and Europe are represented by 76 and 31 samples,
respectively (Table S1). The Chattian and especially the early Chat-
limestones and do not allow morphometrical analysis.
To allow comparison with previous results and include mea-
these studies were included in this study. All the analysis were per-
formed on proloculus size, number of nepionic chambers, number
of secondary chamberlets in the fourth and fifth annular chamber,
diameter of the test at the first annular chamber and number of
macrospheric, generation. Measurements for most of the samples
have been updated, but a number of samples were not accessible,
so could not be re-measured and measurements were used as pre-
sented in cited literature (Table S1). These sources only present
average, range and variation of each character. Therefore, morpho-
logical data for the new measurements were averaged per sample
for each character as well. To standardize for variations in absolute
value between characters these were standardised according to the
maximum value (i.e., resulting in a value ranging between 0 and 1).
Although some analytical power might be lost using averages
rather than the raw data, the distribution of morphological data
within most samples is unimodal (Fig. S2). Since stratigraphical
distribution is not good enough to know the relative age of samples
within a stratigraphic bin, specimen based approaches would only
be able to identify the potential presence of multiple species
within samples (e.g., [18]), but it would not be possible to detect
the morphological evolution of single groups. The internal consis-
tency of the data, in which extremes of populations might overlap,
but the average values differ, is used to trace the morphological
evolution of populations.
Stratigraphy
Large benthic foraminifera have long been used as the main
method of biostratigraphical correlation in tropical, shallow, mar-
ine environments (e.g., [10,50,47]). Both combined range zones
and morphometric methods have been applied. Correlation
between regions was done by assuming that evolutionary trends
were synchronous over large geographical areas (e.g., [16]). Recent
advances in stratigraphy, such as the application of Sr-isotope stra-
tigraphy and an increasing number of sections in which both
planktonic foraminifera and large benthic foraminifera have been
observed, allow the reconstruction of an independent geochrono-
logical framework, enabling the assessment of morphological

A B C D

1 mm 2 mm 1 mm 0.5 mm

Fig. 3. (A) Cycloclypeus annulatus (TF521, East Kalimantan, Indonesia, late Middle Miocene, RGM 791539) showing the annular ridges on the exterior of the test, (B)
Cycloclypeus carpenteri (SS07G07, Great Barrier Reef, Australia; Recent, RGM791541) showing the smooth exterior morphology of the other lineages, (C) Cycloclypeus
koolhoveni, thin section, (Tji Apus, Java, Indonesia, middle Oligocene), and (D) Cycloclypeus mediterraneus, thin section (SP707, Villajoyasa, Spain, late Oligocene, RGM791538).
 W. Renema / GeoResJ 5 (2015) 12–22
Fig. 4. Temporal variation in proloculus size and number of nepionic chambers in four lineages of Cycloclypeus. Samples with abundant specimens without annular chambers
are marked by ⁄. The error bars observe the range of the measurements. To the right the ages of the distribution maps in Fig. 5 have been indicated. Data sources for this graph
are shown in Fig. S3 and Table S3.
change and evolutionary processes over time and space. Although
in this study large benthic foraminifera zonations have been used
to asses ages, neither the occurrence of Cycloclypeus, nor biometric
methods have been taken into account.
The samples used in this study originate from three sources: (1)
museum and new field collections that have not been published
hitherto; (2) samples that have been published before, but have
been re-measured or placed in a revised stratigraphical context;
and (3) published samples that were originally described in suffi-
cient detail.
Single morphological species in a time interval
Coherence of morphological species was tested by determining
the clustering of samples in morphospace within a single strati-
graphical bin. When more than one species is present at the same
time it is expected that they plot with little or no overlap [18]. A
cluster analysis (hierarchical clustering, Euclidian distance, group
average) followed by a similarity profile (SIMPROF) test was used
to test whether multiple species were present in a single strati-
graphical bin. SIMPROF tests whether the coherence within a clus-
ter is larger than expected by randomly selecting the same number
of samples from the entire dataset (maximum 1000 runs, p = 0.05)
[13]. Regions used to label the samples were Europe, Pacific, Aus-
tralia, and Indonesia. If multiple species occur within a strati-
graphic bin, it is expected that statistically different clusters
occur in morphospace. Alternatively if only a single species occurs
no significant clustering should be found.
15
Temporal trends in morphological variation
Hypothesis testing becomes increasingly complicated when
species show morphological change over time (phyletic change)
and even more so during speciation events, since any a-priori,
often subjective, grouping will affect the outcome of the analysis.
I have tested for temporal variation in morphology by testing for
correlation between proloculus size, sp4+5, and X with the median
age of the sample.
All analyses were performed using PRIMER 6.1.6.
Results
Frequent occurrence of convergent evolution, resulting in mac-
roscopically identical tests (e.g., the presence of operculine, heter-
ostegine, and annular chambers) have muddied the classification
and evolutionary understanding of large benthic foraminifera.
Hence, internal structures of the test are important characters for
higher levels of classification. These include the connections
between chambers, and within the chambers between chamber-
lets, or stolons. These can be observed as apertures in the chamber
and chamberlet walls. A second important structure are the canals
within the chamber walls. These can only be observed in well
preserved specimens. The canal system in Cycloclypeus consists of
parallel marginal canals as well as two parallel canals in the
chamberlet walls. Representatives of all lineages reported in this
study have pairs of radial stolons on either side of the secondary
septa, underpinning the assumption that Cycloclypeus is a
16 W. Renema / GeoResJ 5 (2015) 12–22

Fig. 5. Geographic distribution of species in the genus Cycloclypeus during the Oligocene–Recent. (A) Early Rupelian; (B) late Rupelian–earliest Chattian; (C) middle Chattian;
(D) late Chattian; (E) Aquitanian; (F) early Burdigalian; (G) late Burdigalian/early Langhian; (H) late Langhian/Serravallian; (I) Late Miocene; (J) Pliocene. Open circles
represents localities with samples in suitable facies types, but without Cycloclypeus. Arrows indicate most important range expansions/contraction and the red dotted line in
(I) and (J) indicates the current distribution of Cycloclypeus.

monophyletic group. At least within the Early Miocene and youn- chambers, in the Rupelian of Spain, Turkey, and Indonesia, often
ger specimens no annular stolons were observed. erroneously referred to as Heterostegina (or Planostegina), might
The occurrence of populations consisting at least partly of only indicate that these two lineages derived independently. Differ-
operculine and heterostegine chambers, thus lacking annular ences in the morphology of the secondary chambers, but even
 W. Renema / GeoResJ 5 (2015) 12–22
more the presence of interpolated chambers and the thick and
irregular chamber wall in the European populations might support
this interpretation. Unfortunately no specimens with a well-pre-
served canal system were found.
At the species level inconsistent interpretation of existing
names, the erection of new taxa based on environmentally influ-
enced characters, and inconsistent use of names originally assigned
to microspheric or macrospheric forms have resulted in a taxo-
nomic mess. Several authors (e.g., [54,37,44]) distinguished sepa-
rate lineages or forms based on surface ornamentation of the
test. In most populations, however, specimens occur with variable
surface ornamentation, but similar internal morphology [1,34,16],
and here I follow the latter authors by predominantly focusing
on the internal morphology to discriminate between lineages. In
the present paper I recognize four lineages and six species within
the genus Cycloclypeus. The variation in morphological characters
is summarized in Figs. 4 and S3.
Cycloclypeus koolhoveni Tan [53] – Lineage (Fig. 3C)
This lineage constitutes of Rupelian Cycloclypeus with a rela-
tively large proloculus and long, rapidly opening initial spire, with
18–46 nepionic chambers, the average >22 in all populations. In
the oldest populations specimens without annular chambers (Het-
erostegina praecursor Tan of previous authors) are common. The
variation in external morphology includes the presence of an
umbonal thickening (used to recognize Cycloclypeus bantamensis
by Tan [54]). The spiral wall, including the marginal cord, is thin
and regular, as are the secondary chamberlets. Secondary chamb-
erlets are isometric to slightly higher than long in the nepionic
chambers, becoming narrow, up to four times as high as wide. In
specimens with a few nepionic chambers chamberlets in the annu-
lar chambers are isometric to twice as high as long at most Inter-
polated chambers, chambers without apertural chamberlets [34],
are rare.
For only eight samples biometric data are available. These show
an increase in proloculus size, a decrease in the number of nepionic
chambers, and no trend in the number of chamberlets in sp4+5.
Especially in the oldest samples many specimens lack annular
chambers, in these samples X_mean represents the number of nep-
ionic chambers of specimens with annular chambers. In all popula-
tions the distribution of morphological characters is left skewed.
Cycloclypeus pseudocarpenteri Özcan et al. [45]
This species is flat with a distinct central knob and evenly dis-
tributed granules. It has a large proloculus (0.17–0.38 mm), few
(2–5) nepionic chambers, and no or only one undivided initial
chamber. The spiral wall is regular, interpolated chambers have
not been observed, and the chamberlets are isometric in the early
whorls becoming at most twice as high as wide in the later whorls.
C. pseudocarpenteri was originally described from the early Late
Oligocene of Turkey [45]. This species is morphologically similar
to both the Cycloclypeus eidae–C. carpenteri-lineage (especially
the extant species C. carpenteri) and the C. koolhoveni-lineage.
The rapidly opening initial spire, chamberlet shape and external
appearance are more similar to the C. koolhoveni lineage, but there
is a large difference in especially the number of nepionic chambers.
Contemporaneous specimens of the C. eidae-lineage occurring in
Malaysia have a much smaller proloculus and 3–4 times as many
nepionic chambers. The proloculus of the Turkish specimens is
even larger than those of extant C. carpenteri. This combination
of characters suggests that it is more likely that C. pseudocarpenteri
is the youngest representative of the C. koolhoveni lineage, than the
oldest of the C. eidae-lineage.
17
C. pseudocarpenteri was recently described from the early Chat-
tian of eastern Turkey [45]. In Turkey this species was found in the
same sample as Cycloclypeus mediterraneus [45].
Only few occurrences of this species are known, hence it was
not included in the morphological analyses.
Cycloclypeus eidae Tan [53]–Cycloclypeus carpenteri Brady [7] –
Lineage (Fig. 3B)
This lineage constitutes of Chattian to Recent Cycloclypeus. The
oldest representatives have a relatively small proloculus, and a
short, slowly opening initial spire, with 25 or less nepionic cham-
bers. The youngest representatives have a larger proloculus and
only 4–6 nepionic chambers. The chamberlets are very evenly
sized, usually as high as wide. Combined with the more regular
thickness of the marginal cord, and the low number of interpolated
chambers the nepionic stage has a more regular appearance than
the C. mediterraneus lineage. C. eidae is the oldest species of this
lineage, and has a small proloculus, and a larger number of nepion-
ic chambers. C. eidae is found in the Chattian–Burdigalian. The old-
est occurrence is contemporaneous with C. mediterraneus-lineage
and C. pseudocarpenteri. The extant species C. carpenteri occurs in
the Langhian–Recent and has a larger proloculus and smaller num-
ber of nepionic chambers.
Cycloclypeus annulatus Martin [38] – Lineage (Fig. 3A)
Based on the formation of, usually multiple, annular thickenings
of the test C. annulatus is often placed in its own genus or subgenus
Katacycloclypeus Tan [54]. However, Adams and Frame (1979, p.
16) concluded that ‘the mere possession of annular thickenings is
not a diagnostic character at the generic level, although it has sig-
nificance at the species level’. Apart from the annular ridges, the
macrospheric specimens also show an augmented rate of increase
in proloculus size compared to contemporaneous C. eidae/C. car-
penteri. Tan intended to publish a second volume of his monograph
on Cycloclypeus in Indonesia covering the C. annulatus group, but
died before this work was completed. He identified several species
based on the number of annular thickenings of the test with over-
lapping numbers of nepionic chambers. Adams and Frame [1]
found it justified to regard the species with annular thickenings
as a separate lineage within the genus Cycloclypeus, but did not
separate this lineage into multiple species.
Cycloclypeus mediterraneus Matteucci and Schiavinotto [39] – Lineage
These consists of late Rupelian-middle Chattian Cycloclypeus
with a relatively large proloculus and long initial spire, with on
average 12–32 nepionic chambers. Both macrospheric and micro-
spheric forms have a distinct umbonal knob, but the presence of
other ornamentation is very variable. This lineage has isometric
chamberlets in the annular chambers, whereas the contemporary
C. koolhoveni has narrow, elongate chamberlets. The spiral wall,
including the marginal cord, is thick and irregular. Interpolated
chambers are frequent [34]. Several of the oldest populations con-
tain specimens without annular chambers.
Biogeography
The genus Cycloclypeus appears in the early Rupelian (34–31 Ma)
of Java and Kalimantan with the first occurrence of
C. koolhoveni (Fig. 5A). By the end of the Rupelian (30–28 Ma) C.
mediterraneus is recorded from Europe (Fig. 5B), where in the early
Chattian (28–26 Ma) C. mediterraneus was widespread (Fig. 5C).
During the middle Chattian (26–24 Ma), the C. mediterraneus
18 W. Renema / GeoResJ 5 (2015) 12–22
lineage went extinct, followed by a re-immigration of early repre-
sentatives of the C. eidae–C. carpenteri lineage into the Mediterra-
nean area (Fig. 5D) in the last part of the Chattian (24–23 Ma)
[10]. The last occurrence of C. eidae in Europe is marked by a rapid
extinction before the Aquitanian (23–20 Ma) [10], in a period when
C. eidae in the Pacific realm had its most limited north–south dis-
tribution (Fig. 5E). During the Burdigalian (20–16 Ma) and younger,
the geographic range of the C. eidae–C. carpenteri lineage showed
some more fluctuations in both north–south and east–west direc-
tions (Fig. 5F–J), the most notable in the late Burdigalian (18–
16 Ma), when C. eidae–C. carpenteri expanded as far south as south-
ern Australia and New Zealand, that were at even higher latitudes
than they are now. It is noteworthy that the northernmost occur-
rences are reported in the early Burdigalian (20–18 Ma) and Plio-
cene (5.3–2.6 Ma), showing asynchronous excursions to higher
latitudes in the northern and southern hemisphere, probably
related to the intensity of warm water (paleo) Kuroshio, Leeuwin
and East Australia currents [40,19].
Furthermore, the genus Cycloclypeus did not recolonise Western
Australia following its extirpation in the late Serravallian (13.8–
11.6 Ma), even though present day conditions [32] seem suitable
for its occurrence.
Morphological variation
I analysed the morphological evolution in 139 samples covering
the entire geographical and spatial range of Cycloclypeus. Morpho-
metrical data are sparse from most of the (especially northern)
Pacific, where Cycloclypeus was known to occur (Fig. 5).
Morphological variation within time intervals
Cluster analysis followed by a SIMPROF analysis result in one to
three distinct morphological clusters co-occurring in a single
stratigraphic bin (Table 1; Fig. S1). In the middle Chattian (26–
24 Ma) two geographically separated groups (early C. eidae and C.
mediterraneus) evolve independently in the (proto) Mediterranean
area and the West Pacific, respectively. Possibly the youngest rep-
resentatives of the C. koolhoveni lineage occur in the Middle East.
Within C. eidae no structure according to region nor age of the
localities is observed (Table 1; Fig. S1). Within C. mediterraneus
no significant clusters have been found (Table 1; Fig. S1). During
the late Chattian (24–23 Ma) morphological evolution was homo-
geneous over an area stretching from Spain to East Indonesia. In
the Aquitanian two clusters are observed: early C. annulatus which
is restricted to west Indonesia, and C. eidae that is morphologically
homogeneous from East Turkey to the West Pacific islands (Table 1;
Fig. S1). A similar pattern is observed in the Burdigalian
(20–16 Ma). However, the Langhian (16–13.8 Ma) Victorian/South
Table 1
Number of significant clusters in SIMPROF analysis for nine time intervals. Dendrograms are shown in Fig. S1.
Age Number of Number of p Remarks
clusters samples
Late Miocene 1 15 >0.05
Late Middle 2 16 <0.05
Miocene
Early Middle 3 20 <0.01
Miocene
Late Early Miocene 2 12 <0.01
Early Early 2 9 <0.05
Miocene
Late Oligocene 1 10 >0.05
Middle Oligocene 2 12 <0.05
Early Oligocene 2 16 <0.05
Earliest Oligocene 1 8 >0.05
Australian populations are statistically different (and plot interme-
diate between C. eidae and C. carpenteri).
Temporal trends in morphological variation
In samples of two (C. annulatus and C. mediterraneus) of the
three analysed lineages proloculus size, sp4 5, and X are positively
correlated with median age (Fig. 6). This is consistent with Hunt
[30] who found significant directional morphological evolution in
the C. mediterraneus-lineage based on the data of Laagland [34],
which have been included in this study as well. When all samples
in the C. eidae–C. carpenteri lineage are included in the analysis a
weak significant correlation is found, but the lineage can be sepa-
rated into two lineages with a non-significant correlation that dif-
fer in proloculus size, separated by intermediate samples from the
Burdigalian/Langhian (18–15 Ma) in southern Australia. The speci-
mens with a small sized proloculus are included as C. eidae,
whereas those with a large proloculus are placed in the extant C.
carpenteri. In sections from Java, Kalimantan, and Sulawesi cover-
ing this time interval the C. eidae–C. carpenteri transition can be
observed in subsequent lithological units. C. eidae is associated
with planktonic foraminifera indicative of M8, whereas C. carpen-
teri is associated with planktonic foraminifera indicative of M9.
C. eidae–C. annulatus speciation
Variation within most samples is unimodal and left skewed,
sometimes with a long tail (e.g., Fig. S2D). However, in the late
Chattian–early Aquitanian (22–18 Ma) two overlapping morpho-
types can be recognized (Figs. 4, S2B and C), one having a large
proloculus and short nepionic spire (type 1), the other a small prol-
oculus and large nepionic spire (type 2). One or two annular ridges
can develop in each morphotype. From some populations measure-
ments were done on X-ray image and the entire test was still avail-
able. Specimens in these samples have been tentatively separated
in a group with at least one annular ridge (placed in the C. annul-
atus-lineage), which have a larger proloculus and left skewed dis-
tribution, and without annular ridges (placed in the C. eidae
lineage), which have a small proloculus and a right skewed distri-
bution. Other populations which could not be separated on exter-
nal characters since only thin sections were available have an
intermediate proloculus size and bimodal distribution. Samples
from other areas in the same time interval have a small proloculus
showing a left skewed unimodal distribution.
In late Burdigalian (18–16 Ma) and younger samples, these two
morphotypes do not overlap and annular ridges develop consis-
tently in specimens of type 1 morphology (the C. annulatus lineage)
and not in the type 2 (C. eidae) lineage.
C. annulatus; Australian–Pacific–Indonesian C. carpenteri; Fijian C. annulatus as an outlier
C. annulatus; west Australian–Pacific–Indonesian C. eidae; southern Australian transitional C.
eidae–C. carpenteri
C. annulatus; European, Australian, Pacific, Indonesian C. eidae
Europe–Indonesia–Pacific C. eidae, west Indonesian transitional population to C. annulatus
European and Indonesian C. eidae, Ghar Hassan (Malta) is an outlier
Indonesian C. eidae and European C. mediterraneus
Indonesian C. koolhoveni and European C. mediterraneus
 W. Renema / GeoResJ 5 (2015) 12–22 19

Fig. 6. Ranked proloculus size versus time in four lineages: (A) C. eidae–C. carpenteri, triangles represent populations with large proloculus, circles with small proloculus, (B) C.
annulatus, (C) C. koolhoveni, and (D) C. mediterraneus.

The C. koolhoveni lineage includes too few samples for this
analysis.
Discussion
The key result of this study is the marked heterogeneity of
speciation modes, patterns of morphological evolution, and
extinction in a single genus of large benthic foraminifera. Both
peripheral (C. eidae–C. carpenteri in southern Australia), vicariant
(C. mediterraneus in the proto Mediterranean), and sympatric
(C. annulatus in Indonesia) speciation has been documented
(Fig. 7). Previously, it was assumed that morphological evolution
in Cycloclypeus lineages is gradual and unidirectional, with not
more than one species co-occurring in each time interval. In the
evidence provided here four lineages and five species can be recog-
nized, with two or three lineages co-occurring during most of the
Chattian to Middle Miocene. In taxa with wide ranging species
an important role is attributed to non-spatially restricted specia-
tion, i.e., the differentiation of geographically isolated populations
into distinct species by barrier formation, that is, allopatry [4],
20 W. Renema / GeoResJ 5 (2015) 12–22
Fig. 7. Schematic representation of morphological variation through time in the
genus Cycloclypeus.
whereas in taxa with restricted ranges, spatially restricted specia-
tion might be most common. Large benthic foraminifera include
mostly wide ranging taxa [35], one of which is C. carpenteri. Below
I will discuss some key aspects of the morphological evolution of
Cycloclypeus.
Modes of speciation
In taxa with wide ranging species an important role is attrib-
uted to non-spatially restricted speciation, i.e., the differentiation
of geographically isolated populations into distinct species by bar-
rier formation, or allopatry [4], whereas in taxa with restricted
ranges, spatially restricted speciation might be most common.
Large benthic foraminifera include mostly wide ranging taxa
[35], one of which is C. carpenteri. However, here I document two
taxa with sufficient spatio-temporal coverage that went through
a period of neo-endemism.
The eidae–annulatus transition matches with the predictions of
sympatric speciation. Initially there is increased variation, followed
by bimodality. This is only observed in that part of the range of the
ancestral species, where the oldest specimens of unmistakably
C. annulatus have been observed. Even though it is likely that
C. annulatus and C. eidae had slightly differing environmental
preferences, this matches with the expectations of geographically
sympatric speciation.
The eidae–carpenteri transition matches the expected pattern of
parapatric speciation (Fig. 1). Variability is comparable in all
populations, but in a restricted, marginal part of the range
intermediate populations between the two species are observed
(Figs. 4 and 5).
The speciation of C. koolhoveni and C. mediterraneus, as well as
the first occurrence of C. eidae can either be interpreted as originat-
ing from an unsampled ancestral population, making it a case of
allopatric speciation, or of repeated evolution of the same
characters. Arguments for the latter includes the presence of inter-
mediate forms between planospiral nummulitids with secondary
chamberlets in both the oldest C. mediterraneus and C. koolhoveni
populations [45,54] lacking annular chambers. In the case of a
monophyletic range expansion into the Mediterranean, this
resulted in morphological evolution which is conform predictions
of allopatric speciation. That such long distance migration does
not have to result in speciation is shown in the Chattian, when C.
eidae migrated from the IWP to the Mediterranean area, but no sig-
nificant differences between these populations were observed.
The key result of this study is the marked heterogeneity of spe-
ciation modes, patterns of morphological evolution, and extinction
in a single genus of large benthic foraminifera. Both peripheral (C.
eidae–C. carpenteri in southern Australia), vicariant (C. mediterran-
eus in the proto Mediterranean), and sympatric (C. annulatus in
Indonesia) speciation has been documented (Fig. 4). The C. koolho-
veni–C. eidae transition has not been observed. The reduction in
proloculus size is unusual since in most larger benthic foraminifera
lineages it is usually assumed that proloculus size unidirectionally
increases over larger time scales (nepionic acceleration; [16]). This
can either be interpreted as an unusual response to, for example,
environmental conditions, or that there is an (unknown) sister spe-
cies that has remained below the radar.
Previously, it was assumed that morphological evolution in
Cycloclypeus lineages is gradual and unidirectional, with not more
than one species co-occurring in each time interval [54,44,16]. In
the evidence provided here four lineages and five species can be
recognized, with two or three lineages co-occurring during most
of the Late Oligocene to Middle Miocene.
Evidence for morphological stability
The C. eidae to C. carpenteri lineage has long been interpreted as
a gradual directional transition from species with a small prolocu-
lus and numerous nepionic chambers, to species with a large prol-
oculus and few nepionic chambers (e.g., [54,44,16]). The data
presented here suggest two independently evolving species with
no or very little morphological change through time over an exten-
sive part of their ranges. Arguably the oldest specimens of both lin-
eages show some morphological change, but the younger samples
are not sorted by time (Fig. 5). This pattern is strongest in C. eidae
(Fig. 5A)
Evidence for gradualism
The C. mediterraneus and C. annulatus lineage both show linearly
arranged samples sorted by time (Fig. 5B and D). Also within sec-
tions (e.g. the Lanuza section of Laagland [34]) this directional
trend was observed [30].
Evidence for peripheral speciation
The co-occurrence of both C. eidae and a morphological inter-
mediate population in southern Australia, interpreted to be early
C. carpenteri (Figs. 4 and 5) and the morphological stability in C.
eidae and C. carpenteri for a period of 12–14 My do not conform
to the expectations of gradual evolution in a single directional
trend in the C. eidae–C. carpenteri lineage. Here I propose an alter-
native scenario of pulsed evolution of C. carpenteri in a relatively
short time span. Speciation was not only temporally restricted to
the Langhian but also spatially restricted to southern Australia.
The latter is a peripheral area that could only be colonized because
of the southward expansion of tropical conditions during the Mid-
dle Miocene Climate Optimum [58]. Isolation was attenuated by
the southward proto-Leeuwin and East Australia currents [40,19].
Following climate cooling, especially at higher latitudes, and a
large regression during the Middle Miocene Climate Transition
[58] C. carpenteri disappeared from the ancestral area, but replaced
C. eidae in the tropical Pacific. In conclusion, next to temporally
undersampled punctuations in a temporal analysis, in which a spe-
cies appears to evolve rapidly because the temporal resolution of
samples is too low to capture the gradual transition [31], here I
 W. Renema / GeoResJ 5 (2015) 12–22
demonstrate the possibility of geographically undersampled punc-
tuations, in which morphological change in spatially isolated pop-
ulations is overlooked in geographically restricted studies.
Evidence for sympatric speciation
The C. eidae–C. annulatus cladogenetic event occurred within
the central area of the geographic range of C. eidae and is associated
with an initial increase in variation and bimodal distribution of
morphological characters (Figs. 4 and S2). Speciation in larger ben-
thic foraminifera has been hypothesized to occur along environ-
mental trends, especially depth [24,27]. Other well-documented
examples of sympatric speciation in the fossil record, especially
in planktonic organisms also involve speciation along environmen-
tal gradients [43,29]. Contrary to these studies, speciation in
Cycloclypeus is spatially restricted to a small area, followed by rapid
range expansion of the sister species.
Prolonged coexistence of a bimodal character distribution in
recent populations is observed in hybrid zones [17]. Hybrid zones
occur when genetically distinct groups of individuals meet and
mate, resulting in at least some offspring of mixed ancestry
[2,3,25,9]. Detecting hybrid zones depends on inferring the relative
importance of history and current ecology as explanations for
observed distributions of phenotypes and genotypes [9]. Hybrid
zones have rarely been documented in the fossil record even
though hybridisation is increasingly accepted in extant biota
[20]. Most recent hybrid zones are documented using genetic char-
acteristics. It is to be expected that hybrid zones in the fossil record
are equally important, but failed to be detected due to a number of
reasons: (1) the fossil record lacks the resolution required to inter-
pret speciation on a meaningful time-scale; and (2) it is difficult to
disentangle genetic from environmental influences [22,20]. Docu-
mented cases of hybridisation in the fossil record all involve sec-
ondary hybridisation, in which two well defined species mix as
the result of removal of a barrier and result in species with inter-
mediate characters [20].
A primary hybrid zone results from differentiation among a ser-
ies of connected populations that can lead to striking variation in
multiple characters. Character distribution is predicted to be bimo-
dal, variation is higher compared to the ancestral and successor
populations, and the hybrid zone should be spatially restricted
[17]. Primary hybridisation can result in speciation, and often
occurs along environmental gradients. The observed pattern in
character variability in the C. eidae–C. annulatus-speciation event
match the predictions of Endler [17], but compared to documented
examples it has a very long duration, and no evidence of genetic
mixing can be presented.
Evidence for geologically instantaneous extinction
In at least one case in Cycloclypeus (C. mediterraneus), extinction
was instantaneous (within detection limits) over its entire range
and probably associated with a reduction in either depth of the
photic zone or steepening of the bathymetric temperature profile
in its range, likely as a result of a change in ocean circulation pat-
terns. Following recolonisation, C. eidae showed a similar pattern in
the Mediterranean area just a few millions later, but persisted in
the Indo West Pacific. Species specialized in extremes of environ-
mental gradients, such as Cycloclypeus, are more sensitive to such
changes than eurytopic species [49,28].
Implications
There is an increasing use of molecular phylogenetic
approaches to understand the processes resulting in present-day
biodiversity and to infer the timing and geography of speciation
21
events, e.g., Bellwood & Meyer [4], Williams and Duda [57] in the
marine realm, and Smith [51] and Wiens et al. [56] in the terres-
trial realm. These studies use the combination of sister species-
range analysis and accurately dated divergences to identify poten-
tial sites of species origination [4]. Applying this method to C. car-
penteri would result in an inferred location of speciation within its
current range (its sister taxa are even more widely distributed than
Cycloclypeus itself) around the Eocene/Oligocene boundary (34
million years ago), whereas the geological age of the extant species
C. carpenteri is around 16–20 Ma. Applying this method thus
results in a twofold overestimation of the divergence date, due to
the extinction of ancestral species. It also results in a failure to
detect the area of origin, as that is inferred to lie outside its current
distribution range (Fig. 5G).
Morphologic and genetical evolution are not necessarily
directly linked. Since the development of the molecular clock, it
has become apparent that a strict application, with a constant sub-
stitution rate, is in many occasions not applicable. In other words,
it becomes increasingly more evident that substitution rates vary
through time. Here I observe changes in morphological evolution
over both time and space. Using this analogue it could be possible
that genetic substitution rates also vary over space. If that is the
case, this would have implications for using fossils from regions
where the species is now extinct as calibration points.
Conclusion
The dataset presented here forms a complete dataset docu-
menting spatial and geographical variation in morphological char-
acters. These data allow, for the first time, the direct assessment of
speciation processes based on occurrences of fossils in this genus. I
demonstrate that at a single moment in time up to three species of
Cycloclypeus can be present, and that both gradual change (the C.
annulatus and C. mediterraneus lineages) and stasis in morphology
over millions of years are observed (in the C. eidae–C. carpenteri
lineage). Contrary to the generally accepted idea that speciation
in wide ranging taxa predominantly occurs by vicariance, two
out of three speciation events are geographically restricted. C.
annulatus evolved sympatrically in the centre of the range of its
ancestor, whereas C. carpenteri evolved in the periphery of the dis-
tribution of its ancestor.
Geographic variation in morphological characters were alter-
nated with intervals in which morphology was constant over the
entire geographical range. Character evolution during two specia-
tion events could be described in this study. During the C. eidae–
C. annulatus cladogenetic event morphological variation increased,
followed by a bimodal but overlapping distribution, and in the final
phase one species is indistinct from the ancestral species (includ-
ing range of variation) and the second has distinct morphological
characters. This occurred in geographically overlapping areas. The
C. eidae–C. carpenteri speciation event showed a change in mor-
phology without changing variability. This event happened in an
isolated peripheral area, but was followed by rapid range expan-
sion and replacement of the ancestral species.
Despite the low number of species, examples of allopatric,
peripatric, and sympatric cladogenisis were documented, demon-
strating the marked heterogeneity of evolutionary processes and
the difficulty to make assumptions regarding tempo and mode of
evolution.
Multiple phases of range expansion and contraction were
observed, probably moderated by climatic variability, most likely
surface temperature and given their deep habitat, the bathymetric
temperature gradient. Interestingly, expansion to higher latitudes
were not synchronous between the northern and southern
hemispheres.
22 W. Renema / GeoResJ 5 (2015) 12–22
Acknowledgements
The author appreciates the constructive remarks of Gene Hunt
and Briony Louise Mamo that have significantly improved an ear-
lier version of the manuscript.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.grj.2014.11.001.
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