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royalsocietypublishing.org/journal/rsbl
Research
Cite this article: Baxter-Gilbert J, Riley JL,
Wagener C, Mohanty NP, Measey J. 2020
Shrinking before our isles: the rapid expression
of insular dwarfism in two invasive populations
of guttural toad (Sclerophrys gutturalis). Biol.
Lett. 16: 20200651.
http://dx.doi.org/10.1098/rsbl.2020.0651
Received: 5 September 2020
Accepted: 20 October 2020
Subject Areas:
evolution, ecology
Keywords:
amphibian, body size, invasive species,
island biology, morphology
Author for correspondence:
James Baxter-Gilbert
e-mail: jx_baxtergilbert@laurentian.ca
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.5193656.
Evolutionary biology
Shrinking before our isles: the rapid
expression of insular dwarfism in two
invasive populations of guttural toad
(Sclerophrys gutturalis)
James Baxter-Gilbert1, Julia L. Riley2,3, Carla Wagener1, Nitya P. Mohanty1
and John Measey1
1
Centre for Invasion Biology and
2
Department of Botany and Zoology, Stellenbosch University, Stellenbosch,
Western Cape, 7600, South Africa
3
Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada, B3H 4R2
JB-G, 0000-0002-1283-8893; JLR, 0000-0001-7691-6910; CW, 0000-0002-2248-6043;
NPM, 0000-0001-7768-6483; JM, 0000-0001-9939-7615
Island ecosystems have traditionally been hailed as natural laboratories
for examining phenotypic change, including dramatic shifts in body size.
Similarly, biological invasions can drive rapid localized adaptations within
modern timeframes. Here, we compare the morphology of two invasive
guttural toad (Sclerophrys gutturalis) populations in Mauritius and Réunion
with their source population from South Africa. We found that female toads
on both islands were significantly smaller than mainland counterparts (33.9%
and 25.9% reduction, respectively), as were males in Mauritius (22.4%). We
also discovered a significant reduction in the relative hindlimb length of both
sexes, on both islands, compared with mainland toads (ranging from 3.4 to
9.0%). If our findings are a result of natural selection, then this would suggest
that the dramatic reshaping of an amphibian’s morphology—leading to insular
dwarfism—can result in less than 100 years; however, further research
is required to elucidate the mechanism driving this change (e.g. heritable
adaptation, phenotypic plasticity, or an interaction between them).
1. Introduction
Islands have a long history of piquing the interest of evolutionary ecologists,
owing to the frequent stark contrasts between insular and mainland populations
(e.g. divergent behavioural and morphological traits) [1–3]. These island-specific
features can arise from adaptation by natural selection [4–6], phenotypic plas-
ticity [7] or an interplay between them—accelerating adaptation towards
localized ‘optimal’phenotypes [8]. Examining adaptive processes within these
natural laboratories has contributed extensively to our understanding of evol-
ution [1,8] and the concept of island syndromes (i.e. repeated convergent
island-specific traits across species and locations [3,9]). Some of the more com-
monly recognized traits associated with island syndromes involve reduced
antipredator behaviour, longer life spans, lower reproductive outputs and
dramatic changes in body size (e.g. the ‘island rule’—insular dwarfism in
large-bodied species and island gigantism in small-bodied species) [3,6,9,10].
For many taxa associated with the island syndrome, phenotypic change occurs
after colonizing islands through island biogeographic processes [11,12], like the
oversized and fearless Dodos (Raphus cucullatus) of Mauritius or the miniature hip-
popotamuses (Hippopotamus creutzburgi) and elephants (Mammuthus creticus)of
Pleistocene Crete [3]. Yet within the modern era, anthropogenic introductions of
species outside their native range occur far more frequently [13]. The establishment
and success of invasive species represent additional opportunities where we can
© 2020 The Author(s) Published by the Royal Society. All rights reserved.
observe rapid phenotypic changes [14,15]. Given the role
humans play in the spread of invasive species [13] and the recur-
rent negative impacts [16], detailed information on the origin,
timeframes and local ecological interactions is generally well
known. This can provide fine-scale temporal and genetic details
not always available to more traditional island evolutionary
studies. Invasions may also be replicated across multiple
locations, owing to repeating anthropogenic causes (e.g. trans-
portation networks and deliberate introductions [13]), allowing
for parallel investigations into island-derived phenotypic
change to provide deeper insights.
Compared with other vertebrate groups (e.g. birds, mam-
mals, and reptiles) [1–10], amphibians have received less
attention regarding island-derived morphological changes
[17–19]. This taxonomic bias is surprising, as studies on
mainland amphibians have greatly advanced our understand-
ing of rapid phenotypic change during invasions [20] and
dramatic changes in size (e.g. miniaturization) have naturally
evolved numerous times across several lineages [21,22]. Here,
we examine the morphology of guttural toads (Sclerophrys
gutturalis) within their invasive populations on the islands of
Mauritius and Réunion, after almost 100 years of colonization,
and compare them with their known mainland source popula-
tion in South Africa [23]. We test whether relatively parallel
toad invasions have resulted in comparable phenotypic diver-
gence in overall body size, skull shape and limb lengths. Based
on preliminary reports from Mauritius [24], and following
trends seen in other bufonid populations invading tropical
islands [18], we predict that guttural toads on both islands
will exhibit reductions in overall body size, when compared
with the native mainland counterparts, and their skull shape
and limb lengths to scale proportionately.
2. Methods
(a) Study system
Guttural toads are large bufonids, up to 140 mm snout–vent
length (SVL) [25], with a broad distribution in sub-Saharan
Africa [23] (figure 1a,b). These toads also have invasive popu-
lations in Mauritius, Réunion and Cape Town (South Africa; see
electronic supplementary material for more details), with a mol-
ecular analysis confirming that all three invasive populations
have the same native source population originating near
Durban, South Africa and that the founding populations on Maur-
itius and Réunion had a relatively high degree of genetic diversity
[23]. Their deliberate introduction to Mauritius occurred in 1922,
and toads were subsequently moved from Mauritius to Réunion
in 1927 [23,26] (figure 1b), resulting in both invasions experiencing
island-specific selective pressures for roughly 47 generations [27].
Mauritius and Réunion are similarly sized islands, 2040 km
2
and 2512 km
2
respectively [23], that have tropical climates. Ecolo-
gically, both are considered biodiversity hotspots that are rich
in endemics [28] and lack any recent evolutionary history
with bufonids (pre-1920’s [26]). Although not identical, these
islands represent two relatively similar ecosystems, sharing a
wide diversity of flora and fauna, including invertebrate commu-
nities [29–31] (prey for toads [24]) and similar toad predators
(mostly non-native vertebrates [26]).
(b) Data collection
We caught adult guttural toads from multiple sites in Mauritius
(two sites; n= 158 toads), Réunion (two sites; n= 186) and in and
around Durban, South Africa (four sites; n= 151) between June
2019 and March 2020 (see electronic supplementary material for
the region and sex-specific details). Upon capture, we recorded
each toad’s collection site and sex, and took morphological
measuresof SVL, jaw width, jaw length, forearm length (combining
upper and lower forearm lengths), hindlimb length (combining
upper and lower hindlimb lengths) and foot length, using a set of
digital callipers (±0.01 mm). All measurements were taken by the
same researcher (JB-G) on the toad’s left side (unless prior injury
prevented it; n= 2) to avoid interobserver variation.
(c) Statistical analysis
Owing to known sexual size dimorphism in anurans, including
bufonids [32], we accounted for sex-specific differences in our
analyses. Before analyses, all morphological traits were log
10
transformed to ensure allometric relationships were linear [33].
Durban
80
60
40
1927
1922
snout–vent length (mm)
Mauritius Réunion
location
(a)
(b)
(c)
Figure 1. Guttural toads (a) are native to mainland Africa (shaded pink [23] in b) and were introduced from Durban, South Africa, to Mauritius in 1922 and then to
Réunion in 1927 (b). Between these locations, snout–vent length (SVL; mm) differed based on location and sexes (c). Depicted are raw SVL for each location by sex
(females in beige and males in green). Significant differences in female and male toads between locations are shown using a beige and a green line, respectively,
along the x-axis with squares at the ends. Sex-specific differences at each location are shown with a black line with beige and green squares at the ends located
above the boxplots. The figure depicts raw data points on the left with corresponding boxplots.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 16: 20200651
2
Using linear mixed effect models (LMM), we examined whether
there were differences in adult toad SVL between locations, sex
and an interaction between location and sex. In the LMM, we
also included the random intercept of the collection site to
incorporate dependency among toads from the same population.
We then used separate LMM that contained the same fixed,
interaction and random effects as the LMM analysing SVL to
examine differences in five other morphological traits ( jaw width,
jaw length, forearm length, hindlimb length and foot length).
In addition, these LMM included the fixed factor of SVL to test
for potential changes in these five morphological traits that are dis-
proportionate to any changes in toad SVL. Post-hoc we tested for
multiple comparisons between study locations and sexes correct-
ing p-values using the Scheffe procedure [34] (see electronic
supplementary materials for additional details).
3. Results
All model outputs and additional information on the location
and sex-specific differences in morphology are presented in
the electronic supplementary materials.
(a) Female toads
Female toads from Mauritius and Réunion had significantly
shorter SVL than Durban by 33.9% and 25.9%, respectively
(figures 1cand 2a). Controlling for SVL, Réunion females had
significantly shorter jaw lengths than females from Durban
(by 4.5%) and Mauritius females had significantly shorter
forearmsthan Durban females (by 8.8%; figure 2). Also, females
from Mauritius and Réunion had significantly shorter
hindlimbs and feet than Durban females, independent of
reductions in their SVL (figure 2). Mauritius female hindlimbs
and feet were shorter than those of Durban females by 7.1%
and 14.9%, respectively (figure 2). Réunion female hindlimbs
and feet were shorter than those of Durban females by 4.5%
and 8.8%, respectively (figure 2).
(b) Male toads
Male toad SVL from Mauritius was significantly shorter (22.4%)
than those of Durban males (figures 1cand 2a), a trend not
seen with Réunion males. Males from Mauritius and Réunion
had shorter hindlimbs (by 9.0% and 3.4%, respectively) than
Durban males, disproportionate to differences in their SVL
(figure 2). In addition, males from Mauritius and Réunion
differed in their hindlimb length; males from Mauritius have
hindlimbs that are 5.8% smaller than Réunion males. Foot
length of Mauritius males was 16.8% shorter, also accounting
for SVL, than that of Durban males (figure 2) and Mauritius
male foot length was significantly shorter than the foot length
of Réunion males (by 8.8%).
4. Discussion
Mauritius and Réunion guttural toad populations have experi-
enced substantial reductions in overall body size compared
with their source population in Durban; however, the extent of
change varies between the sexes and islands. We observed
further reductions in skull and limb lengths, accounting for
SVL, but these too varied between sexes and locations. Notably,
we observed significant reductions in hindlimb length, dispro-
portionate to SVL, across both sexes and islands compared
with mainland counterparts. Owing to the high degree of gen-
etic diversity on both islands [23] and historical practices for
deliberately introducing large numbersof amphibian biocontrol
agents [26,36], we assert that our findings are not a result of
50
40
30
20
10 DMR DM R DMR DMR DMR
jaw width jaw length forearm
length
hindlimb
length
foot length
DMR DM R DMR DMR DMR
jaw width jaw length forearm
length
hindlimb
length
foot length
length or width (mm)
50
40
30
20
10
mor
p
holo
g
ical traits
decrease of...
Durban
female toads
male toads
Mauritius Réunion
0–5% 5–10% 10–15% 15–20% 20–25% 25–30% 30–35%
(a)(b)
(c)
Figure 2. The degree to which morphological traits decreased in reference to female and male toads from the native, source population in Durban (a). Snout–vent
length (SVL) is represented using a rectangle along the toad’s midline. Percentage decreases in morphological traits were calculated separately for each sex and were
based on statistically significant differences between estimated marginal means (EMM [35]) generated from their respective LMM. In addition, morphological trait
( jaw width, as well as jaw, forearm, hindlimb and foot lengths) EMM and 95% confidence intervals are shown for female (b) and male toads (c) from Durban
(‘D’, green), Mauritius (‘M’, orange) and Réunion (‘R’, purple). Significant differences between locations are shown using grey straight lines that are ended with
squares reflecting the colours of each location.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 16: 20200651
3
founder effects (for more details, see electronic supplementary
materials), yet we are unable to determine the evolutionary
mechanisms of this change (e.g. adaptation or phenotypic plas-
ticity). Even if this ‘island morphology’is, or originally was, a
product of phenotypic plasticity, this still can result in heritable
adaptations arising through avenues such as ‘plasticity-first’
adaptation [37], heritable phenotypic plasticity [38], or by
acting as a stopgap allowing populations to persist long
enough for natural selection to take place [39,40]. Overall,
what we are able to report is a highly rapid response (less
than 100 years) compared with previous studies on island-
derived changes in amphibian body size that report timescales
for colonization and isolation that are two to five orders of mag-
nitude longer [17–19,41]. This suggests that dramatic changes in
body size, related to island populations, can arise rapidly soon
after establishment.
The reduction in body size was more pronounced in
Mauritius, both in effect size and occurring in both sexes,
while in Réunion this trend was only significant for female
toads. Sex-specific insular dwarfism in a reptile has been
suggested to be related to localized differences in prey [42];
however, this remains to be tested for guttural toads. In gen-
eral, our findings of reduced body size follow what has been
seen in other tropical island populations of toads (e.g. ornate
forest toad, Rhinella ornata [18]); however, it is in contrast with
reports of amphibian island gigantism from temperate cli-
mates (e.g. green toads, Bufo viridis [41] and rice frogs,
Fejervarya limnocharis [17]). Dichotomous shifts in island
body size in mammals have been suggested to be related to
taxonomic differences in ecology (e.g. local carrying capacity,
resource specificity and/or trophic level) and original main-
land body size [2,6], while in amphibians it may be related
to an island’s climate [17,18]. Island amphibians from more
seasonal climates require larger body sizes to account for
longer periods of inactivity and shorter reproductive seasons
[17], based on the assumption that body size and condition
positively correlate with reproductive output [43,44]. If this
assertion is accurate, then tropical island toad populations
that are active throughout the year, and able to breed over
longer periods, may not have the same restrictions on mor-
phology for breeding success during annual breeding
events (e.g. a capital breeding strategy [45]). Examinations
of the island syndrome have noted that insular populations
can show increases in longevity with smaller reproductive
outputs [3,10]. If this is also true for guttural toads, then
the selective forces maintaining a large body size may have
been relaxed, owing to the populations in Mauritius and
Réunion engaging in smaller, but more frequent, reproduc-
tive bouts (akin to an income-breeding strategy [45]). This
hypothesis does require further research into the evolution-
ary mechanism driving guttural toad’s insular dwarfism, as
well as uncovering any island-specific changes in life-history
strategies and reproductive output.
We also see some variation between sexes and popu-
lations in limb and skull sizes, including a significant
reduction in jaw length for female toads from Réunion com-
pared with Durban and between-island differences in traits
such as male foot length (see electronic supplementary
materials for details). The most prominent change, however,
was the significant reduction in hindlimb length across both
sexes and islands. One possible cause of this could be a
shift in selection associated with predator–prey interactions.
The absence of the toads’native predators may have relaxed
selection on the need to maintain large hindlimbs that pro-
vide longer bounds during escape [46–48], which could
allow energy to be allocated elsewhere, such as more frequent
reproductive events or other physiological processes (akin to
the ‘enemy release hypothesis’[49]). This reduction in limb
length may also be associated with a reduced dispersal abil-
ity, similar to trends seen in island birds (e.g. flightlessness),
as fitness benefits associated with investments in dispersal
are diminished for insular populations [3,9,50]. As such, the
reductions in body size and shape may be a result of selective
forces favouring a less dispersive morphological phenotype
[51]. Further research is required, however, comparing pred-
atory selective pressures between mainland and island
populations, as well as research on differences in locomotory
performance and behaviour.
Miniaturization has repeatedly evolved within amphibian
clades [21,22] and examples of dramatic shifts in amphibian
body size have also been seen on islands [17–19,41] and
mountains [52], yet these changes are typically reported
within the context of thousands or millions of years. Our
study suggests that a reduction in body size by up to a
third can occur in less than a century—representing an excep-
tionally rapid expression of this trait. These findings mirror
the rapid formation of distinct morphologies arising within
lizard populations introduced to islands, either experimen-
tally or through other anthropogenic activities [15,53,54]. If
this holds true more broadly across other insular taxa, includ-
ing those observed in the fossil record, then island-derived
phenotypes may arise at a much faster rate than commonly
assumed. We hope this study leads to further research atten-
tion being given to this relatively understudied invasive
amphibian [55] within Mauritius and Réunion, particularly
as this toad’s introduction to these globally important bio-
diversity hotspots [28] may yield further insights into the
pace at which islands can drive evolution.
Ethics. This work was conducted with authorization from Ezemvelo
KwaZulu-Natal Wildlife (Ordinary Permit: OP 4072/2019) and
Mauritian National Parks and Conservation Services (NP 46/3 V3),
as well as with Stellenbosch University Research Ethics Committee
clearance (ACU-2019-10386).
Data accessibility. The datasets and R code for this study are available
from Open Source Framework (OSF) at https://osf.io/hw3fm/
(doi:10.17605/OSF.IO/HW3FM) [56].
Authors’contributions. J.B.-G. and J.M. conceived and designed the pro-
ject. J.B.-G., J.L.R., C.W. and N.P.M. collected the data. J.L.R. led
the statistical analysis and drafted the corresponding sections of the
manuscript. J.B.-G. led the initial drafting of the manuscript. All
authors contributed to, and have approved, the final manuscript
and agree to be held accountable for the content of this paper.
Competing interests. We declare we have no competing interests.
Funding. J.B.-G., C.W., N.P.M. and J.M. would like to thank the
DSI-NRF Centre of Excellence for Invasion Biology for their
support. J.L.R. was supported by postdoctoral fellowships from the
Claude Leon Foundation and the Natural Sciences and Engineering
Research Council of Canada (NSERC). This research was also
funded through an African Collaborations Grant awarded to J.B.-G.
and J.M. from the Centre for Collaboration in Africa at Stellenbosch
University.
Acknowledgements. We would like to thank C. Baider, V. Florens,
P. Kowalski, M. Campbell, M. Mühlenhaupt, S. Peta, R. Wedderburn,
S. Sauroy-Toucouère, D. Strasberg and A. Cheke for their invaluable
support, as well as three anonymous reviewers. We would also like to
thank BlackRiver Gorges National Park, the DurbanBotanical Gardens,
Amatikulu Nature Reserve and the communities of Notre Dame, Villèle
and Pont Payet.
royalsocietypublishing.org/journal/rsbl Biol. Lett. 16: 20200651
4
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