How the temperate world was colonised by bindweeds: Biogeography of the Convolvuleae (Convolvulaceae)

Abstract

Background
At a global scale, the temperate zone is highly fragmented both between and within hemispheres. This paper aims to investigate how the world’s disjunct temperate zones have been colonised by the pan-temperate plant group Convolvuleae, sampling 148 of the c. 225 known species. We specifically determine the number and timing of amphitropical and transoceanic disjunctions, investigate the extent to which disjunctions in Convolvuleae are spatio-temporally congruent with those in other temperate plant groups and determine the impact of long-distance dispersal events on diversification rates. ResultsEight major disjunctions are observed in Convolvuleae: two Northern Hemisphere, two Southern Hemisphere and four amphitropical. Diversity in the Southern Hemisphere is largely the result of a single colonisation of Africa 3.1–6.4 Ma, and subsequent dispersals from Africa to both Australasia and South America. Speciation rates within this monophyletic, largely Southern Hemisphere group (1.38 species Myr−1) are found to be over twice those of the tribe as a whole (0.64 species Myr-1). Increased speciation rates are also observed in Calystegia (1.65 species Myr−1). Conclusions
The Convolvuleae has colonised every continent of the world with a temperate biome in c. 18 Myr and eight major range disjunctions underlie this broad distribution. In keeping with other temperate lineages exhibiting disjunct distributions, long-distance dispersal is inferred as the main process explaining the patterns observed although for one American-Eurasian disjunction we cannot exclude vicariance. The colonisation of the temperate zones of the three southern continents within the last c. 4 Myr is likely to have stimulated high rates of diversification recovered in this group, with lineage accumulation rates comparable to those reported for adaptive radiations.

Full text

RES E A R C H A R T I C L E Open Access
How the temperate world was colonised by
bindweeds: biogeography of the
Convolvuleae (Convolvulaceae)
Thomas C. Mitchell
1*†
, Bethany R. M. Williams
2†
, John R. I. Wood
2
, David. J. Harris
3
, Robert W. Scotland
2
and Mark A. Carine
4
Abstract
Background: At a global scale, the temperate zone is highly fragmented both between and within hemispheres.
This paper aims to investigate how the world’s disjunct temperate zones have been colonised by the pan-temperate
plant group Convolvuleae, sampling 148 of the c. 225 known species. We specifically determine the number and
timing of amphitropical and transoceanic disjunctions, investigate the extent to which disjunctions in Convolvuleae are
spatio-temporally congruent with those in other temperate plant groups and determine the impact of long-distance
dispersal events on diversification rates.
Results: Eight major disjunctions are obser ved in Convolvuleae: two Northern Hemisphere, two Southern
Hemisphere and four amphitropical. Diversity in the Southern Hemisphere is largely the result of a single colonisation
of Africa 3.1–6.4 Ma, and subsequent dispersals from Africa to both Australasia and South America. Speciation rates
within this monophyletic, largely Southern Hemisphere group (1.38 species Myr
−1
) are found to be over twice those of
the tribe as a whole (0.64 species Myr
-1)
. Increased speciation rates are also observed in Calystegia (1.65 species Myr
−1
).
Conclusions: The Convolvuleae has colonised every continent of the world with a temperate biome in c. 18 Myr and
eight major range disjunctions underlie this broad distribution. In keeping with other temperate lineages exhibiting
disjunct distributions, long-distance dispersal is inferred as the main process explaining the patterns observed although
for one American-Eurasian disjunction we cannot exclude vicariance. The colonisation of the temperate zones of the
three southern continents within the last c. 4 Myr is likely to have stimulated high rates of diversification recovered in
this group, with lineage accumulation rates comparable to those reported for adaptive radiations.
Keywords: Amphitropical, Calystegia, Convolvulus, Disjunction, Diversification rates, Polymeria, Temperate, Transoceanic
Background
The successful colonisation of temperate biomes by trop-
ical lineages has involved the crossing of a significant
physiological barrier that has acted as an important filter
[1]. As a consequence, approximately half of all plant fam-
ilies remain restricted to the tropics [2]. Lineages that have
made the transition to temperate biomes have experienced
different fates with some lineages expanding their ranges
to occupy highly disjunct areas where a suitable climate
occurs, with distributions spanning both different con-
tinents and different hemispheres. Whilst the processes
responsible for such patter ns ar e complex [3–6], long-
distance dispersal (LDD) event s have been proposed for
many such disjunctions and they may have acted as
triggers for diversification [7, 8].
Thorne [9] recognised fifteen temperate disjunction
patterns, several of which have since been the focus of
molecular phylogenetic studies to understand the extent
to which vicariance and dispersal explain biogeographic
patterns in temperate plant lineages (e.g., the eastern
North American–E ast Asian disjunction [10]; the tem-
perate North and South American disjunction [11]; the
western North American–East Asian disjunction [12]).
* Correspondence: tom.mitchell@tum.de
†
Equal contributors
1
Plant Biodiversity Research, Technische Universität München, Emil-Ramann
Strasse 2, 85354 Freising, Germany
Full list of author informa tion is available at the end of the article
© 2016 Mitchell et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Mitchell et al. BMC Evolutionary Biology (2016) 16:16
DOI 10.1186/s12862-016-0591-6

One of the patterns documented by Thorne [9] was the
‘North–South Temperate disjunction’ which describes
groups that are widespread in the northern temperate
region and that also occur in one or more of the southern
temperate zones (i.e., those located in South America,
Africa and Australasia).
The Convolvuleae (Choisy) Choisy is one of 12
tribes within the predominantly tropical plant family
Convolvulaceae Juss. [13]. It is one of only two tribes
withinthefamilytohavewidelycolonisedtemperate
regions (the other being the parasitic Cuscuteae) and it
exhibits Tho rne’s ‘North–south Temperate disjunction’
pattern. The Convolvuleae comprises three genera
namely Convolvulus L., Calystegia R.Br. and Polymeria
R.Br.. Convolvulus is the largest, comprising 190 spe cies
[14]. It has a main centre of diversity in the Mediterranean
and western Asia, with further centres of diversity in
eastern Asia and in temperate South America, southern
and eastern Africa and Australasia; i.e., the three temperate
zones of the southern hemisphere. Species also occur in
North America, although they are few in number. Calyste-
gia is readily distinguished from Convolvulus based on
morphological characters (namely polypantoporate pollen
and stigma shape) but molecular analyses suggest it is
nested within the larger Convolvulus clade [13, 15, 16].
Calystegia is taxonomically complex [17] with c. 26 species
and more than 65 distinct taxa currently accepted [18].
The centre of diversity for Calystegia is in California where
nearly half of the described taxa occur [19]. Other centres
of diversit y for Calystegia are found in eastern Asia and, to
a lesser extent Europe and the Mediterranean. Calystegia
also occurs in temperate regions of the Southern
Hemisphere. Finally, the Australasian endemic Polymeria is
the smallest of the three genera of Convolvuleae with eight
species recognised [18]. Molecular analyses place it as sister
group to the remainder of Convolvuleae [13, 15, 16].
A recent study by Williams et al. [16] established a
robust phylogenetic hypothesis of the Convolvuleae that
sampled 62 % of species diversity in the tribe and was
based on data from both the nuclear ITS region and the
chloroplast matKandrbcL regions. The goal of this paper
is to utilise that phylogenetic framework to determine how
the North–South Temperate disjunction pattern displayed
by Convolvuleae was generated. Specifically, we aim to (i)
determine the number, timing and cause (dispersal versus
vicariance) of amphitropical and transoceanic disjunctions
in the pan-temperate Convolvuleae and (ii) determine how
major disjunctions in the history of the group may have
impacted on diversification rates.
Results
Convolvulaceae–solanaceae analysis
An alignment comprising 153 species of Convolvulaceae
(of which 109 were Convolvuleae; eight Polymeria,11
Calystegia,90Convolvulus) and 343 species of Solanaceae
(126 Solanoideae) and 1328 characters from the matKand
rbcL regions (of which 538 were parsimony informative)
was used to establish divergence times within Convolvula-
ceae. The rbcL region was coded with missing data for 241
taxa, of which four were Convolvuleae. A chronogram with
major groups is summarised in Additional file 1. The Con-
volvulaceae are resolved to have arisen 44.1 (95 % HPD
33.9–51.2) Ma, in agreement with Särkinen et al. [20]. Age
estimates established for nodes within Solanaceae are also
in agreement with Särkinen et al. [20]. Within Convolvula-
ceae, the Convolvuloideae sensu Stefanović et al. [21] is
resolved as 20.9 (14.3–27.5) Myr old, with the Convolvu-
leae crown group ( corresponding to the split between Poly-
meria and the Convolvulus + Calystegia clade) resolved at
17.9 (11.8–23.7) Ma.
Convolvuleae analysis
Five areas of endemism within Convolvuleae were
delimited using UPGMA clustering of species by country
distribution data (Fig. 1a). A Convolvuleae alignment
consisted of 148 species of Convolvuleae (11 Polymeria,
18 Calystegia, 119 Convolvulus) and 2033 characters
from the rbcL, matK and ITS regions (matrix deposited
in TreeBASE, study 18623). Divergence times estimated
in BEAST using calibration points derived from the
Solanaceae-Convolvulaceae analysis above and ancestral
area reconstructions estimated using LAGRANGE are
provided in Fig. 1b with Table 1 summarising the infor-
mation for key nodes of interest.
The ancestral area of the Convolvulus + Calystegia clade
is inferred to be the Mediterranean-and-Middle-East (area
A in Fig. 1a; node 2). Dispersal between contiguous areas
(i.e., A–B, A–C, C–D (Fig. 1a)) occurred frequently (Fig. 1b).
Movement between disjunct (i.e., non-contiguous) areas
has been much less common and eight such events are
inferred. These are, in order of recency: (i) amphitropical
disjunction between Australasia (Area G) and the
Mediterranean-and-Middle-Ea st (Area A) (posterior
probability for node (PP) = 1) dated 17.61 Ma (95 %
highest posterior density (HPD): 13.50–21.56 Ma)
(node 1; Fig. 1b; Table 1), (ii) Northern hemisphere
disjunction between the Mediterranean-and-Middle-
East (A) and North America (F) (PP = 1) dated 5.92 Ma
(3.53–8.6 Ma) (node 16), (iii) Northern hemisphere dis-
junction between Central-and-North-Eastern-Asia (B) and
North America (F) (PP = 1), dated 5.56 Ma (3.45–8.26 Ma)
(node 12), (iv) amphitropical disjunction between the
Mediterranean-and-Middle-East (A) and Southern-and-
Eastern-Africa (D) (PP = 1) dated 4.62 Ma (3.12–6.41 Ma)
(node 5), (v) transoceanic southern hemisphere disjunction
between Southern-and-Eastern-Africa (D) and Australasia
(G) (PP = 1), dated 3.06 Ma (1.99–4.41 Ma) (node 6), (vi)
weakly supported transoceanic southern hemisphere
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 2 of 12

Fig. 1 (See legend on next page.)
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 3 of 12

disjunction between Southern-and-Ea stern-Africa (D)
and South America (E) (PP = 0.52) dated a s 1.15 Ma
(0.65–1.78 Ma) (node 8), (vii) weakly supported (PP = 0.59)
amphitropical disjunction between South America (E) and
North America (F), dated 0.57 Ma (0.18–1.03 Ma) (node 9)
and (viii) weakly supported (PP = 0.79) amphitropical
disjunction between North America (F) and the Southern
Hemisphere (Australasia (G), South America (E) or both,
node 15), dated 0.82 Ma (0.3–1.53 Ma)
Diversification rate analysis
BAMM analysis found support for rate shifts within the
Convolvuleae phylogeny compared with a single rate
model (Bayes factors (BF) > 30 for 2–6 shifts). The max-
imum a posteriori (MAP) probability rate shift configur-
ation, which alone explains 56 % of the data , infers two
rate shifts: one on the stem branch of the southern
hemisphere clade (Fig. 2; group A; BF = 755) and one on
the stem branch of Calystegia (Fig. 2; group B; BF = 424)
(Additional file 2a). Mean speciation rates (λ) within the
circum-South Temperate (cST) clade (1.38, 90 % HPD:
0.71–2.07) and Calystegia (1.65, 90 % HPD: 0.61–2.73)
are over twice those of the tribe as a whole (0.64, 90 %
HPD: 0.5–0.83). Extinction rates (μ) however are also
slightly higher in both the cST clade (0.47, 90 % HPD:
0.04–1.19) and Calystegia (0.86, 90 % HPD: 0.14–2.07)
than in Convolvuleae as a whole (0.31, 90 % HPD: 0.11–
0.58). Mean d iversification rates (λ - μ)inthecSTclade
(0.91 species Myr
−1
) are therefore nearly three times greater
thaninthetreeasawhole(0.34speciesMyr
−1
), while those
in Calystegia are over twice as fast (0.8 species Myr
−1
)as
Convolvuleae in general. Extinction rates are inferred to
have remained fairly constant over the history of the tribe,
however speciation rates appear to ha ve increased consider -
ably in the last 2.5 Myr (Additional file 2b).
Discussion
Both the world’s oceans and the equatorial tropics
present barriers to dispersal of temperate lineages, po-
tentially limit ing exchange between the disjunct temper-
ate zones of the world. In Convolvuleae, we observe four
amphitropical an d four transoceanic disjunctions in the
history of the group with an increase in diversification
rate associated with one amphitropical disjunction (the
main group of Convolvulus in the southern hemisphere).
A second increase in diversification rate is observed in
Calystegia which also exhibits a transoceanic disjunction.
The four amphitropical disjunctions are spread through-
out the history of the tribe (Fig. 1b, nodes 1, 5, 9 and 16).
The earliest dates to the mid-Miocene (17.61 (13.5–21.56)
Ma;node1;Fig.1b;Table1)andseparatestheAustralasian
endemic Polymeria from the remainder of Convolvuleae
(Convolvulus + Calystegia), for which the Mediterranean-
and-Middle-East is resolved as the ancestral distribution
area. T his spatio-temporal pattern is consistent with the
inferred timing of the disjunction between Australia and
Eurasia in Carex subsect. Spirostachyae (c.16–26 Ma [22])
and in Halosarcia (c.15–20 Ma [23]). Escudero et al. [22]
invoked LDD to explain this disjunction although the tim-
ing is coincident with the mid-Miocene Climatic Optimum
15–17 Ma, which saw the expansion of tropical forests, an
event that is thought to have facilitated the dispersal of
tropical plant and animal groups between Africa and Asia
[24]. It is plausible that a corresponding contraction of
temperate areas may have led to the disjunction apparent
in these groups. S ärkinen et al. [20] resolved a similar sister
grouprelationshipinSolanum between the Western
Mediterranean–Macaronesian endemic Normania clade
and the Australasian endemic Archaesolanum clade
and an Australian– No rther n Hemisphere disjunction
was also infe rred for Atr iplex [25].However,thetiming
of these was more re c ent (8.3 Ma and 9.8–7.8 Ma re-
spectively) suggesting that the history of Australasian–
Northern Hemisphere disjunctions is comp lex with
multiple, temporally distinct events likely involved.
A second amphitropical disjunction in Convolvu-
leae is the result of t he colonisation of the Southern
Hemisphere by Convolvulus during the late Miocene
to Pliocene c.4.62(3.12–6.41) Ma (node 5; Fig. 1b;
Table 1). The most probable scenario involves dis-
persal from the Mediterranean-and-Middle-East into
Southern-and-Ea stern-Africa , followed by dispersal
from there to Australasia c.3.06(1.99–4.41) Ma
(node 6) and South America c.1.15(0.65–1.78) Ma
(node 8) although the precise relationships of African and
American taxa are not well supported. The mountains of
the East African rift system, which link Southern Africa
with the Horn of Africa are thought to have originated c.
12–40 Ma [26] and they provide a plausible trans-African
dispersal corridor for Convolvuleae as has been suggested
for other temperate taxa (e.g., Senecio [27]; Disa, Irideaeae
(See figure on previous page.)
Fig. 1 Phylogeny of Convolvuleae. a) Map depicting the areas of endemism for Convolvuleae delimited using UPGMA analysis. b) Dated phylogeny of
Convolvuleae inferred in BEAST from analysis of the concatenated ITS, matKandrbcL dataset. Node bars represent 95 % HPD estimates. Scale bar
represent millions of years before present. Coloured branches and taxon names indicate the distribution area inferred in LAGRANGE, as shown in Fig. 1a.
Black branches indicate ambiguous areas (less than 0.2 lnL difference between first and second most likely distribution). Grey branches indicate a multiple
area distribution. Numbers at the top-left of nodes a re referred to in Table 1. * indicate the loca tion of calibr ated nodes. Black circles on nodes
indicate nodes with Bayesian Posterior Probabilities of at least 0.95
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 4 of 12

Table 1 Biogeographical inference and minimum age estimates for key nodes
LAGRANGE analysis Molecular dating using BEAST
Node Split lnL Rel. Prob. Node BPP Node age (Myr) 95 % HPD (Myr) Notes
1 G/A −219.5 0.5948 1 17.61 13.50–21.56 Convolvuleae crown group. Disjunction (i).
G/AC −221.3 0.1036
2 A/A − 219.6 0.565 1 15.89 12.32–19.46 Convolvulus + Calystegia crown group.
3 A/A − 220.3 0.2739 1 7.34 4.8–10.55
A/ADG −221.5 0.08379
ABC/A −221.6 0.07558
A/AD −222.1 0.04663
AC/A − 222.1 0.04593
AB/A −222.1 0.04531
A/ABD −222.2 0.0.04
4 A/A − 220.3 0.2915 1 5.55 3.72–7.74
A/ADG −220.9 0.1506
A/AD −221.0 0.1379
A/ABD −221.0 0.132
A/ABG − 221.7 0.06887
A/AG − 221.8 0.06279
A/AB −221.8 0.06069
5 D/AB − 220.3 0.2897 1 4.62 3.12–6.41 Stem of Southern Hemisphere group. Disjunction (ii).
DG/A −220.3 0.2887
D/A −220.7 0.1846
G/AB −221.1 0.1196
G/A −222.1 0.04466
6 G/D −219.1 0.9433 1 3.06 1.99–4.41 Crown group of the circum-South Temperate (cST group),
Southern-and-Eastern-African to Australasia. Disjunction (iii).
7 D/D −219.1 0.9326 1 2.28 1.46–3.31 Southern-and-Eastern-African and South American crown group.
8 D/E −219.1 0.9557 0.52 1.15 0.65–1.78 Southern-and-Eastern-African to South American movement. Disjunction (iv).
9 F/E −219 1.0 0.59 0.57 0.18
–1.03 South America to North America movement. Disjunction (v).
10 A/A −219.8 0.4384 1 8.55 5.62–11.74 Calystegia and allies crown group.
A/AB −220.2 0.297
A/B −220.8 0.1656
11 AB/B −219.5 0.5995 0.47 7.85
B/B −220.9 0.1513
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 5 of 12

Table 1 Biogeographical inference and minimum age estimates for key nodes (Continued)
12 BF/A −219.9 0.4336 1 5.56 3.45–8.26 Central-and-North-Eastern-Asia to North America movement, Calystegia stem.
Disjunction (vi).
B/A −219.9 0.3958
13 F/BF −219.5 0.6076 1 2.06 1.28–3.06 Calystegia crown group.
F/BCF −220.3 0.2656
14 F/B −219.9 0.4225 0.66 1.55 0.88–2.36
F/BC −220.2 0.3018
BF/B −220.6 0.2156
15 EFG/G −219.5 0.5969 0.79 0.82 0.3–1.53 Stem node of clade with Amphitropical American to Southern Hemisphere
movement (South America and Australasia). Disjunction (vii).
FG/G −220.0 0.3934
16 A/F −219 1.0 1 5.92 3.53–8.6 Mediterranean-and-Middle-East to North America disjunction. Disjunction (viii).
LAGRANGE optimisations and BEAST minimum age estimates for key nodes in the Convolvuleae analysis. Node numbers are labelled in Fig. 1b. LAGRANGE splits refer to areas shown in Fig. 1a in the format x/y where x relates
to the top branc h, and y relates to the bottom branch exiting the labelled node. Log likelihoods (lnL) and relative probabilities (Rel. Prob.) are given for each LAGRANGE optimisation within two lnL of the most likely split
optimisation. Bayesian Posterior Probabilities (BPP), mean node ages and 95 % highest posterior density (HPD) estimates inferred in BEAST are given for each node
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 6 of 12

p.p., Pentaschistis, Restionaceae [28]; Androcymbium [29];
Scabiosa [30]). It is notable that whilst some African
amphitropical disjunctions are inferred to be pre-Pliocene
(e.g., Juniperus, 30.5 (14.0–47.0) Ma [31]; Hyacinthoideae,
18.7 (18.8–18.7) Ma [32]; Thamnosma, 8.7 (5.3–12.1) Ma
[33]), Plio– Pleistocene disjunctions, consistent with that
observed in Convolvuleae have been reported in a number
of groups. For example, colonisation of southern Africa
from the north through this corridor has been inferred in
Apium (4.1 (1.2–7.0) Ma [34]), Ranunculus (3.9 (2.6–5.3)
Ma [35]) and Scabiosa (1.6 (0.7–2.6) Ma [30]) whilst South
to North colonisation has been inferred for Androcym-
bium (4.0 (2.5–5.5) Ma and 3.0 (1.5–4.5) Ma [25]) and,
very recently in Senecio (0.2 (0–0.4) Ma [27]).
The remaining amphitropical disjunctions are observed
in the New World. Pleistocene dispersal (0.57 (0.18–1.03)
Ma) from South America to North America is inferred in
the cST group (node 9; Fig. 1b; Table 1). A southwards
dispersal in Calystegia (node 15) is inferred to have oc-
curred at a similar time c.0.82(0.3–1.53) Ma resulting in
the colonisation of South America and Australasia. How-
ever, limited support (Convolvulus; PP = 0.59, Calystegia;
PP = 0.79) or taxonomic uncertainty (Calystegia)means
that these patterns should be interpreted with caution and
the evolution and biogeography of the Calystegia clade in
particular would benefit from further research.
These limitations notwithstanding , amphitropical
American disjunctions of recent origin have been inferred
in a range of groups with evidence for dispersal in both
directions [4]. Bird mediated dispersal has frequently been
proposed as responsible for such disjunctions due to the
seasonal migration of birds between the Northern and
Southern hemispheres (e.g., [11, 36, 37]). Whilst evidence
for this is largely anecdotal, epizoochoric bird-mediated
LDD between California and Chile has been demonstrated
in Lepidium [36]. In the case of Convolvulus, viable seeds
of Convolvulus arvensis have been recovered from the
digestive tract of migratory killdeer (Charadrius vociferus)
up to six days after ingestion [38]. Importantly however,
long-distance internal transport of seeds, even in generally
larger waterbirds has been shown to be limited to around
300 km making extreme long-distance endozoochoric
dispersal unlikely [39]. Montane South American species
of
Convolvulus such as C. crenatifolius and C. montanus
are frequently found above 1500 m [14] and the Andean
high mountains, which are of late Miocene origin [40],
may have provided a suitable route for the dispersal of
temperate Convolvuleae lineages across the neotropics.
Remarkably few transoceanic dispersal events are neces-
sary to explain the global distribution of the Convolvuleae,
in contrast to groups such as Fabaeae [41]. Between the
major Southern Hemisphere landmasses, we infer only two
such dispersal events which both occurred 0.65–4.41 Ma,
long after the breakup of the Gondwanan landmass and
too recent to involve an Antarctic corridor [42]. Divergence
time estimates for southern temperate plant groups
B
A
Fig. 2 The maximum a posteriori probability rate shift configuration inferred by BAMM. The maximum a posteriori probability rate shift configuration
inferred by BAMM analysis of the Convolvuleae concatenated ITS, matKandrbcL dataset. Branches are coloured according to the rate inferred along
that branch. Speciation rates are given as species Myr
−1
. Two rate shifts are inferred: a) the stem branch of the circum-South Temperate clade (Bayes
factor 755); b) the stem branch of Calystegia (Bayes factor 424)
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 7 of 12

indicate a wide range o f ages, with Convolvu leae dis-
junctions among the most recent [ 42]. Whilst detailed
information on dispersal mechanisms within the tribe
are lacking , the variability o f seed characteristics in
Convolvulaceae [43] and e vidence of long-distance
oceanic seed dispersal elsewhere in the family [44] an-
ecdotally support an oceanic dispersal hypothesis for
the Southern Hemisphere distribution of Convolvuleae.
Two independent events in the late Miocene/Pliocene
are inferr ed to be responsible for the earliest colonisa-
tion of North America. The most likely scenario for the
Calystegia clade is dispersal from the Mediterranean-
and-Middle-E ast into Eastern Asia c. 7.85 Ma (node 11;
Fig. 1b; Table 1) and from the re into North America c.
5.56 (3.45–8.26) Ma (node 12). The East Asian–North
American disjunction is one of the best studied disjunc-
tions with numerous examples of movement between
the two regions throughout the Cenozoic [10]. The con-
tinents of the Northern Hemisphere were connected
until 5.4–5.5 Ma when the Bering Land Bridge joining
North America and Eastern Asia was finally severed [45]. A
circum-Arctic floral region spanning this landmass prior to
the severing of the land connections is frequently hypothe-
sised as responsible for both the similarity and diversity of
the flora in these regions (e.g., [9, 31, 46–48]). Given our
estimated age for the Northern Hemisphere disjunction in
Convolvuleae we are unable to reject a vicariance hypoth-
esis for the origin of Calystegia in North America, in con-
trast to all other disjunctions we have inferred.
In the case of Convolvulus simulans (node 16), dispersal
directly from the Mediterranean-and-Middle-East to North
America c. 5.92 (3.53–8.6) Ma is inferred. A disjunction
between the Mediterranean regions of North America and
Europe (Madrean–Tethyan) is well documented (see [5])
and long distance dispersal to North America from the
Mediterranean during the late Miocene/Pliocene has been
inferred in a number of lineages (e.g., Exaculum/Schenkia–
Zeltnera c.9Ma[49],Crocanthemum–Hudsonia c.5.2–
9.2 Ma [50], Eobassia/Chenolea/Spirobassia –Neokochia c.
8.8–13.1 Ma [51]).
With regards widespread and naturalised Convolvulus
that were excluded from our analyses, comparison between
the phylogeny estimated in Williams et al. [16] and our bio-
geographic inference suggests that both excluded species
(C. arvensis and C. lineatus) probably originated in the
Mediterranean-and-Middle-East region.
The diversification rate analysis reveals mean diversifica-
tion rates for Convolvuleae of 0.34 species Myr
−1
,above
the estimated diversification rates of angiosperms as a
whole (0.077–0.089 species Myr
−1
, [52]. Furthermore, two
shifts to increased diversification rates are supported
within the tribe, with strong support for a rate shift in the
southern hemisphere clade (Fig. 2; group A) leading to
mean diversification rates (0.91 species Myr
−1
)which
exceed those of adaptive radiations such as the Hawaiian
radiation of Bidens (0.3–0.8 species Myr
−1
) [7]. BAMM
suggests the elevated diversification rates are linked to an
increase in speciation rate as opposed to a decrease in
extinction rate ( Table 2). The southern hemisphere clade
contains at least two long-distance oceanic dispersal
events within the Southern Hemisphere (nodes 6 and 8;
Fig. 1b; Table 1) and at least two amphitropical dispersal
events (nodes 5 and 9), with the shift to elevated diversifi-
cation rates associated with the initial dispersal into the
southern hemisphere in the late Miocene or Pliocene. This
is consistent with other studies demonstrating the impact
of Miocene dispersal events important in promoting
diversification [8, 53].
The second diversification rate shift is observed in
Calystegia. BAMM finds support, albeit less strongly, for
a shift to increased diversification rates on the stem
branch of Calystegia (Fig. 2; group B), leading to mean
diversification rates (0.8 species Myr
−1
), over twice as
high as those found in Convolvuleae as a whole. Most of
the divers ity of Calystegia is in North America and spe-
cifically California [19] and dispersal from East Asia into
North America, again in the Miocene/Pliocene could
also have been an important trigger for diversification
within the group.
Conclusions
In summary, our results indicate that the Convolvuleae
has successfully colonised every continent of the world
with a temperate biome in c. 18 Myr. The tropics and
major oceans have been significant dispersal barriers for
the group with only eight major disjunctions underlying
this broad ‘North– south temperate’ distribution pattern.
In keeping with many other disjunct temperate lineages,
long-distance dispersal is inferred as the main process
explaining the patterns o bser ved although for one
American-Eurasian disjunction we cannot exclude vic-
ariance resulting from the severing of the Bering L a nd
Bridge. Even though dispersal is the primary process gen-
erating the patterns observed, spatio-temperal congruence
Table 2 Convolvuleae diversification rates
Parameter Convolvuleae Clade A Clade B
λ mean 0.6415216 1.383068 1.658275
5 % 0.5002688 0.7070913 0.6142909
95 % 0.8320921 2.0741443 2.7378688
μ mean 0.3056936 0.4715051 0.8596539
5 % 0.1067923 0.0443146 0.1363267
95 % 0.5751786 1.1944557 2.0701412
Mean net diversification (λ-μ) 0.335828 0.9115629 0.7986211
Estimated mean 90 % HPD (Highest Posterior Density) speciation (λ),
extinction (μ) and net diversification rates inferred in BAMM for Convolvuleae,
and two clades with shifts to increased diversification rates (Fg. 2; A and B).
Rates are given in species Myr
−1
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 8 of 12

is observed with other temperate disjunct groups suggest-
ing a common explanation for the patterns observed. The
Convolvuleae exhibits high diversification rates overall
when compared to other angiosperm groups and the col-
onisation of the temperate zones of the three southern
continents within the last c. 4 Myr is associated with an
increase in diversification rate with lineage accumulation
rates in the clade comparable to those reported for adap-
tive radiations. The Calystegia clade also exhibits a high
diversification rate which probably reflects rapid diversifi-
cation following colonisation of western North America.
The Convolvuleae thus provide a striking example of the
ability of temperate lineages to rapidly colonise highly
disjunct areas worldwide and to diversify.
Methods
Divergence time estimation
The fossil record of Convolvulaceae is poor with none of
the fossils assigned to the family (Convolvulites orichitus
[54], Tricolpites trioblatus [55], C alystegiapoll is microe-
chinatus (in [56]) able to be accurately placed within a
phylogeny. We therefore adopted a two-step calibration
procedure. We first utilised a recent phylogenetic study
of Solanaceae, the sister group to Convolvulaceae [20]
which reviewed all 50 of the known fossils assigned to
the family, a s the basis for calibration points for diver-
gence time estimation within Convolvulaceae based on
chloroplast data. Second, node age estimates from the
chloroplast phylogeny were used to calibrate a combined
nuclear ITS and plastid matK and rbcL phylogeny of
Convolvuleae.
matK and rbcL sequences for C onvolvuleae from
Williams et al. [16] were manually aligned with se-
quences of the same regions for ta xa across the re-
mainder of the Convolvulaceae and Solanaceae, which
were retrie ved f rom GenB ank. Details of all accessions
sampled are included in Additional file 3. The data set s
were concatenated, with ta xa l acking mat K sequences
excluded and taxa lacking rbcL sequences coded with
missing data for this region. Due to the lower l evels of
variationintherbcL region [16] the missing data is
unlikely to have any s ignificant impact on the t ree top-
ology, as it will be overridden by the signal from the
matK region [57].
Following Särkinen et al. [20], we used two calibration
points reflecting the youngest age estimates of the oldest
assignable fossils to constrain (i) the stem node of Solanoi-
deae with a lognormal offset of 23.0 Ma, mean of 0.01, and
standard deviation (SD) of 1.0 and (ii) the Solanaceae stem
node with a lognormal offset of 46.0 Ma, mean of 0.01, and
SD of 1.0. A gamma distribution (shape 0.001, scale 1000)
was used as a prior for the mean mutation rate. Bayesian
time estimation with an uncorrelated lognormal relaxed
clock model was implemented in BEAST v1.8 [58]. Two
independent Markov Chain Monte Carlo (MCMC) runs of
200 million generations, sampling every 10,000 generations
were conducted using a Speciation: Birth–Death process
tree prior and the GTR + I + G model. A run sampling only
from the prior probabilities was also performed to evaluate
the performance of the priors. Mixing of the chains and
convergence were assessed using TRACER v1.6 [59] as was
confirmationofaneffectivesamplesize(ESS)inthepost
burn-in samples exceeding 200 for all estimated parame-
ters. T he output tree fi les were combined using LOGCOM-
BINER v1.8 (part of the BEAST software package)
discarding the first 10 % of trees of each run as burn in.
TREEANNOTATOR v1.8 (part of the BEAST software
package) was used to combine post burn-in trees from the
two runs, calculate the maximum clade credibility tree and
the mean 95 % higher posterior density (HPD) intervals of
node ages. Final trees were edited in FIGTREE v 1.4.0 [60].
A second divergence time analysis was performed on a
concatenated ITS, matKandrbcL dataset modified from
Williams et al. [16] since the ITS region included greater
taxon sampling within Convolvuleae (see Additional file
3 for sampling details). Due to the separate modes of
evolution, the manually aligned matrix was partitioned into
nuclear and plastid regions and parameters estimated inde-
pendently. Analysis in BEAST followed the protocol for the
Convolvulaceae–Solanaceae analysis except that minimum
age estimates from the aforementioned analysis were used
to constrain the Convolvuleae root node and Polymeria,
Convolvulus + Calystegia and Calystegia crown nodes with
normally distributed prior at 17.89 Ma (SD = 3.0), 4.76 Ma
(SD = 1.5), 15.18 Ma (SD = 2.5), and 2.7 Ma (SD = 0.8)
respectively, with the distribution reflecting the 95 % HPD
estimates, and MCMC runs were reduced to 20 million
generations, sampling every 1000 generations.
Biogeographic analysis
The extant distributions of all accepted taxa at a country
level were collated, largely from Wood et al. [14]. Wide-
spread taxa and those for which the natural distribution
may have been obscured by frequent introductions/nat-
uralisations (Convolvulus arvensis, Convolvulus lineatus,
Calystegia soldanella, Calystegia pulchra, Calystegia
sepium subsp. sepium, Calystegia sepium subsp. roseata
and all Calystegia silvatica subspecies) were excluded as
were countries with only a single taxon present. Areas of
endemism were then delimited using Unweighted Pair-
Group Method with Arithmetic Mean (UPGMA) cluster-
ing of a taxon × country distribution matrix using the
Sørensen–Dice coefficient [61, 62] in DENDROUPGMA
[63]. Seven areas were delimited (Fig. 1a) and each taxon
was coded as belonging to one or more of these regions.
Given our use of country borders as opposed to ecological
boundaries to delimit areas, we only considered range
shifts between non-contiguous regions as disjunctions.
Mitchell et al. BMC Evolutionary Biology (2016) 16:16 Page 9 of 12

The historical biogeography of the Convolvuleae was
reconstructed using the dispersal–extinction–cladogen-
esis (DEC) model implemented in LAGRANGE v 2.0.1
[64], with taxon distributions coded as above. Three
time slices were incorporated into the DEC model
reflecting the presence or absence of Northern Hemisphere
land connections between the Old and New Worlds. Subse-
quently, Northern America was isolated from the rest of
the Northern Hemisphere 0–5.5 Ma, a connection existed
between North America and Asia via the Bering Land
Bridge (BLB) 5.5–15 Ma, and a connection also existed
between North America and Europe via the North Atlantic
Land Bridge (NALB) 15–25 Ma. All possible area combina-
tions were permitted throughout. Dispersal probabilities
followed Mao et al. [65], however given the relatively young
age of Convolvuleae, and the subsequent reduction in
major continental movements we simplified the model
from five to three dispersal probabilities: 1.0 for connected
areas , 0.1 for widely disjunct area s and 0.5 for three
combinations of narrowly disjunct areas (area A–area
D, area B–area F and area E–area F, Fig. 1b).
Diversification rate analysis
Bayesian Analysis of Macroevolutionary Mixtures (BAMM)
v2.0 [66] was used to model the dynamics of speciation and
extinction on the time-calibrated Convolvuleae phylogen-
etic tree. Incomplete and non-random taxon sampling was
incorporated directly into the likelihood calculations by
utilising the r ecent monograph of Convolvulus [14] to place
missing taxa into their respective clades. Two independent
BAMM metropolis-coupled MCMC (MCMCMC) runs,
with three heated and one cold chain, were run for 10
million generations and sampled every 1000 generations.
Convergence of BAMM runs was assessed by computing
ESS of log-likelihoods and numbers of shifts using the
CODA library for R: both parameters had effective sample
sizes > 1000. The first 10 % of samples were discarded as
burn-in. Post-run analysis and visualisation was performed
using the R package BAMMtools v2.0 [67].
Additional files
The data sets supporting the results of this article are
available in the TreeBASE repository, study 18623; http://
purl.org/phylo/treebase/phylows/study/TB2:S18623 and
the following additional files.
Additional file 1: Dated phylogeny of Convolvulaceae and
Solanaceae inferred in BEAST from analysis of the concatenated
matK and rbcL dataset. Node bars represent 95 % HPD estimates.
Bayesian Posterior Probabilities (BPP) ≥ 0.95 are given by their respective
nodes. Scale bar represents millions of years before present. * indicate the
location of fossil-calibrated nodes (Särkinen et al. [20]). + indicate the location
of nodes used to calibrate the Convolvuleae phylogeny. (PDF 87 kb)
Additional file 2: BAMM outputs. Phylorate plots (2a) and speciation
rate through time curve for Convolvuleae (2b). Additional file 2a
represents the distinct shift configurations that account for 95% of the
probability of the data (f-values denote the posterior probability of each shift
configuration). Branches are scale colour-coded to indicate rate variation from
red (acceleration) to blue (deceleration). Circles indicate the location of core
rate shifts and are similarly colour-coded, with circle size proportional to the
marginal probability of a shift. Additional file 2b represents a speciation rate
through ti me curve (red) for Convolvuleae. Blue shading represents the
confidence on sp eciation rate at any point in time. (ZIP 474 kb)
Additional file 3: List of accessions included in this study. GenBank
numbers are provided in the respective columns. A dash indicates that
no sequence data was included for that region. (DOCX 26 kb)
Competing interests
The authors declare that they have no competing interests.
Authors’ contributions
MAC, RWS, JRIW and DJH conceived the ideas; TCM, BRMW and JRIW
collected the data; TCM, BRMW and MAC analysed the data and led the
writing. All authors read and approved the final manuscript.
Authors’ information
The authors have broad interests in plant taxonomy, evolution and
biogeography. This study formed part of a collaborative project to
monograph Convolvulus.
Acknowledgments
This work was supported by the German Research Foundation (DFG) and the
Technische Universität München within the funding programme Open
Access Publishing. This study was partially funded by a Syntax grant. We
gratefully acknowledge the Natural History Museum (London), Royal
Botanical Garden Edinburgh and Royal Botanical Gardens, Kew for providing
accesses to herbarium specimens and tissue and the staff of the Molecular
Biology Laboratories and the Wolfson-Wellcome Sequencing Facility at the
Natural History Museum for technical support.
Author details
1
Plant Biodiversity Research, Technische Universität München, Emil-Ramann
Strasse 2, 85354 Freising, Germany.
2
Department of Plant Sciences, University
of Oxford, South Parks Road, Oxford OX1 3RB, UK.
3
Royal Botanic Garden
Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK.
4
Department of Life
Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD,
UK.
Received: 30 October 2015 Accepted: 12 January 2016
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