JHR 42: 93-— I 05 (20 I 5) or JOURNAL OF A peer-reviewed open-access journal
doi: 10.3897/JHR.42.8754 REVIEW ARTICLE (4) Hymenoptera

http://jhr.pensoft.net The international Society of Hymenoptersts. RESEARCH

Polistinae biogeography in the Neotropics:
history and prospects

Antonio F, Carvalho!”, Rodolpho S. T. Menezes**, Alexandre Somavilla’,
Marco A. Costa?, Marco A. Del Lama!

| Universidade Federal de Séo Carlos, Departamento de Genética Evolutiva e Biologia Molecular, Via
Washington Luts, Km 235, Sado Carlos, Séo Paulo, Brazil 2 The City University of New York, Department
of Biology, 160 Convent Avenue, New York, NY, USA 3 Universidade Estadual de Santa Cruz, Rod. Jorge
Amado, Km 16, Ilhéus, Bahia, Brazil 4 Department of Entomology, National Museum of Natural History,
Smithsonian Institution, 10th St. & Constitution Avenue, NW, 20560, Washington, D.C., USA 5 Instituto
Nacional de Pesquisas da Amazonia, Avenida André Araujo, 2936, Aleixo, Manaus, Amazonas, Brazil

Corresponding author: Antonio F Carvalho (carvalhoaf@ufscar.br)

Academic editor: W. Pulawski| Received 15 October 2014 | Accepted 14 December 2014 | Published 18 March 2015
http://zoobank. org/3 LAZECF8-F232-409E-825D-97FBD902914E

Citation: Carvalho AE, Menezes RST, Somavilla A, Costa MA, Del Lama MA (2015) Polistinae biogeography in the
Neotropics: history and prospects. Journal of Hymenoptera Research 42: 93-105. doi: 10.3897/JHR.42.8754

Abstract

Discussions regarding Polistinae biogeography in the last two decades rarely associated current patterns
of distribution with environmental changes. This well-known and very diverse group of insects is highly
endemic in the Neotropics, but environmental factors influencing the enormous biological diversity in
the region are not well established. Exploring evidence on the two main hypotheses concerning the origins
and early colonization processes of paper wasps we position in favor of the Gondwanan hypothesis and
discuss change-promoter processes in the Neotropics whose effects might have altered the distributions
and facilitated the speciation of Polistinae in the region. Furthermore, based on recent advances in bioge-
ography, mostly in the integration of ecological and evolutionary information, we highlight directions for

future biogeographical research within the group.

Keywords

Biological richness, ecology, evolution, paper wasps, speciation, species distribution

Copyright Anténio F Carvalho et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

94 Antonio E Carvalho et al. / Journal of Hymenoptera Research 42: 93-105 (2015)

Introduction

It is surprising how young the biogeography of Polistinae is. Many questions remain
unsolved or have never been posed for this subfamily. This gap in our knowledge
is partially due to the absence of discussions linking variations (e.g., morphological,
molecular and physiological) with historical processes. Exciting themes such as colo-
nization routes, population genetics and phylogeography have not been featured in
discussions of paper wasps’ biology, thereby seriously limiting our ability to draw evo-
lutionary conclusions. Furthermore, many recent advances in science have not been
applied to the study of these insects. For example, it is not known how distributions
of Polistinae species have changed during the Late Cenozoic or if existed and where
refuges were located for forest-dwelling species during periods of extreme cold (i.e., the
ice ages). These issues have already been explored and explanations have been proposed
for some amphibians (Carnaval et al. 2009), birds (Batalha-Filho et al. 2012; Mal-
donado-Coelho 2012), ants (Resende et al. 2010) and plants (Pinheiro et al. 2013).
Also, population relationships and historical demography are unknown for the sub-
family Polistinae.

Compared with Africa, Europe and Asia, regions where paper wasps are abundant,
an endemism of nearly 70% (~630 species) is recorded in the Americas (Richards 1978,
Jeanne 1991, Silveira 2008) and most of the species are restricted to the Neotropics. In
fact, these insects constitute a well-represented group in the Neotropical region, both
in terms of abundance and richness. In addition, differences regarding both nest and
body morphological traits and behavioral strategies (e.g., necrophilia, cyclic oligogyny)
indicate that the region is the main hotspot for Polistinae or, using the words of O. W.
Richards, is “the metropolis of social wasps” (Evans and West-Eberhard 1970).

Despite this richness, biogeographic studies related to Polistinae are not common.
In fact, discussions regarding the origins and distribution patterns of this subfamily
were not discussed by almost two decades; the last study on this subject before Silva
and Noll (2014) was published by Carpenter (1996). However, factors related to the
current distribution and success of paper wasps are typically associated with environ-
mental conditions (e.g., Dejean et al. 2011). In addition, the historical reasons regard-
ing the irradiation of these insects in the Neotropics — i.e., the explosion of species
richness, likely during the Cenozoic — have not been discussed.

Many unanswered questions regarding the biogeography of these interesting insects
can be posed: (1) what evidence exists supporting the biogeographical hypotheses on
the origins of Polistinae and colonization of the New World?, (2) what are the primary
ecological and environmental constraints shifting the distributions of the wasps and
promoting changes in the Neotropics that make it “the metropolis of social wasps”?
and (3) how did these wasps proceed while colonizing the New World? In this work
we focus on the first two questions; the later is the theme of another ongoing study. In
order to address these questions, we provide a brief review of the two main hypotheses
regarding Polistinae biogeography (i.e., the Beringian and Gondwanan hypotheses)
and associate historical processes such as climatic-vegetational changes, orogeny and

Polistinae biogeography in the Neotropics: history and prospects 95

global temperature oscillations with the promotion of changes in Polistinae diversity
and distribution in the Neotropics. In the last section of the text, we highlight some
perspectives that are, in our opinion, critical for a deeper understanding of Polistinae
biogeography. We maintain that these perspectives will drive future knowledge in this
field. If we are able to influence ecological and evolutionary integrative discussions
about these wasps, our goals in this work will certainly be achieved.

Biogeographical hypotheses: origins of Polistinae and colonization of the
Neotropics

Early biogeographical hypotheses stated that paper wasps originated in the tropics
based on the high diversity of such insects in the region (Wheeler 1922, Richards and
Richards 1951). The sympatric and restricted occurrence in the oriental tropics of
the three social subfamilies of Vespidae (Stenogastrinae, Vespinae and Polistinae) and
the presence of ancestral forms in nest architecture (West-Eberhard 1969) and basal
morphological traits (Van der Vecht 1965) support assumptions that the Vespinae/
Polistinae split likely occurred in southeastern Asia (Van der Vecht 1965, Richards
1971). According to these assumptions, the dispersion of paper wasps into the New
World occurred twice through the Bering Strait in the Middle Tertiary and the current
distribution therein was likely reached after the last ice age (Richards 1978).

Carpenter (1981) criticized the relation between center of diversity and center of
origin and suggested that the distribution pattern of paper wasps is “widely Gondwa-
nan.” It was also suggested by Carpenter (1993) that the separation between Africa and
South America in the Early Cretaceous (120-100 million years ago; Mya) was an im-
portant event in the evolutionary history of the group. Carpenter (1996) also reviewed
the two main hypotheses of Polistinae biogeography and performed Component Analy-
ses for Polistes Latreille subgenera. Area cladograms presented in that work supported
the Gondwanan distribution of subgenera and rejected the expected dispersion through
the Bering Strait (as defended by Van der Vecht 1965, Richards 1971, 1978).

Other data also support the Gondwanan distribution of paper wasps and we re-
viewed some of these studies, focusing on paleontological, phylogenetic and diver-
gence time evidence.

Fossil records

There are few data related to the paleodistribution of paper wasps based on fossil re-
cords. Despite this fact, important evidence that permits inferences about the biogeo-
graphic hypotheses was obtained by Brown (1941a) with a specimen from the Upper
Cretaceous: a wasp nest comb of Brownichnus favosites (previously treated as genus
Celliforma) from Utah, United States. The specimen shows traits comparable to papery
nests, just like those of Polistes. This finding defined the presence of social behavior in

96 Antonio FE. Carvalho et al. / Journal of Hymenoptera Research 42: 93-105 (2015)

insects earlier than that predicted in that time, from the Eocene to the Cretaceous, but
Brown (1941a) was unable to determine the relationships of the specimen with today’s
social wasps.

After some discussions regarding the classification of such a comb in Bequaert and
Carpenter (1941) and Brown (1941b), Wenzel (1990) confirmed that the comb is in-
deed from a social wasp. Despite the fact that Wenzel (1990) has not been conclusive
about the relationships of B. favosites with present-day groups, the author advocated
that the comb is certainly from a Vespinae or a Polistinae. Moreover, he defended that
if B. favosites is an ancient Polistes, the vicariance hypothesis (i.e., Gondwanan) “should
remain intact.”

Phylogeny

Phylogenetic inferences have provided important information about the evolutionary
history of Polistinae. Carpenter (1991) carried out the first cladistic analysis of the rela-
tionships among the genera of subfamily based on morphological and nest architecture
characters. This analysis placed the cosmopolitan Polistini as the sister group to the
other tribes. Ropalidiini (Old World), Mischocyttarini and Epiponini were grouped in
a polytomy. Wenzel and Carpenter (1994) solved the polytomy by placing Mischocyt-
tarini as an intermediate group and Ropalidiini and Epiponini as more derived groups.
Pickett and Carpenter (2010), however, reviewed several molecular and morphological
characters of Vespidae and placed Ropalidiini as the most basal group, followed by
Mischocyttarini and Polistini + Epiponini as sister tribes.

The evolutionary history of Polistes has been the most thoroughly studied by phy-
logenetic assessments. We reviewed five of the main studies (Carpenter 1996, Zhu et
al. 2000, Arévalo et al. 2004, Pickett and Wenzel 2004, Pickett et al. 2006) and noted
that the Old World subgenera are invariably those at the base of the trees and that the
New World subgenera are derived. We consider this settlement as a strong evidence
for a more recent colonization in the western tropics. Likewise, considering that Mis-
chocyttarini and Epiponini only occur in the Neotropics, and that no fossils of these
groups were recorded outside of this region [following the suggestion of Carpenter and
Grimaldi (1997) in not considering the misidentifications of two Polybia Lepeletier
found in Burnham (1978) from England] and if genus Paleopolistes from France is
not an Epiponini (Perrard & Carpenter, 2014) we are tempted to give credit to the
hypothesis that both tribes arose in the New World after the separation of Africa and
South America (120 Mya).

Divergence time estimates

Ezenwa et al. (1998) raised assumptions that even though the oldest known paper wasp
fossil dates from the Cretaceous (Brown 1941a), the Vespinae/Polistinae split likely

Polistinae biogeography in the Neotropics: history and prospects yep

occurred in the Middle Jurassic (about 175 Mya) and the four tribes arose between
175 and 80 Mya. These assumptions, although not tested empirically, strengthen the
hypothesis of a possible colonization of the Americas in a Gondwanan scenario due the
exclusivity of Mischocyttarini and Epiponini in this region.

Based on these data, we tend to give credence to the Gondwanan hypothesis as
a reasonable and convincing assumption able to explain the origins and colonization
processes of the worldwide Polistinae distribution, as well as early colonization routes.

The life in the metropolis

Distinct from other regions of the globe, the Neotropics are composed of large, hu-
mid forests that have undergone several changes (Hoorn et al. 2010). These forests
harbor most of the paper wasp fauna in the region (Richards 1978). The causes for the
high biodiversity levels in these rainforests have been recurrently associated with envi-
ronmental changes and hypotheses regarding extrinsic processes (non-genetic mecha-
nisms) that facilitate speciation in the biota, mostly in the Amazonian region, have
also been explored in previous studies. Haffer (1997, 2008) provided extensive reviews
concerning these hypotheses and argued that several of them are relevant to speciation
processes in different geological periods of the Cenozoic.

Although environmental processes have not been commonly explored to explain
the diversity of paper wasps in the Neotropics, historical and recurrent events have
certainly provided evolutionary scenarios for adaptive irradiation of this group in the
region. Richards (1978) recognized that climate and vegetation changes in South
America have mixed the distribution of paper wasps during the geologically recent
past of Brazil. Dejean et al. (2011) associated the fluctuation of species richness to cli-
matic phenomena such as El Nifo and La Nifia in French Guiana. However, empirical
analyses and theoretical assumptions regarding environmental factors able to induce
putative alterations in populations of paper wasps have not been sufficiently discussed.
Here, we provide a quick review of the main hypotheses concerning speciation pro-
cesses in the Neotropics. We aim to highlight the major environmental events that
we consider to have been involved in the Neotropical irradiation of Polistinae during
the Cenozoic. Other proposals can be found in the reviews of Haffer (1997, 2008),
including the Gradient, Canopy-density and Museum hypotheses; we opted not to
include these hypotheses in this work because the arguments used to explain speciation
processes are less general in these hypotheses than in those presented here.

Climatic-vegetational changes: the Refuge hypothesis

The Refuge hypothesis predicts the occurrence of putative forest refuges — regions where
forests remain unaltered irrespective of global temperature oscillations — during the Ce-

nozoic and before, i.e., more than 60 Mya (Haffer 1997, 2008). Even so, Haffer (1969)

98 Antonio FE. Carvalho et al. / Journal of Hymenoptera Research 42: 93-105 (2015)

proposed initially that climatic-vegetational changes during the Pleistocene (1.8—0.1
Mya) were the main causes for novelties and speciation processes to arise in the Ama-
zonian rainforest. This idea suffered criticisms (e.g., Bush and Oliveira 2006) and was
not supported by many studies that contested the short timespan for speciation events
predicted initially by the author since most of the Neotropical groups likely arose before
the Pleistocene (e.g., Zink and Slowinski 1995, Costa 2003, Geurgas et al. 2008).

Haffer modified his earlier ideas based mainly on Bennett’s (1990) assumptions
regarding the influences of Milankovitch cycles on communities over a time scale of
20-100 thousand years, or ky. These cycles, caused by alterations in the Earth’s orbit,
would have affected population structures and caused disruptive events in the Neo-
tropical communities and might be the main factors responsible for oscillating the
climate of the planet due to its influence on glacial/interglacial cycles (see Bennett
(1990) for complete explanations on the Milankovitch cycles). In summary, the Ref-
uge hypothesis (Haffer 1997, 2008) is particularly based on the effects of dry/humid
periods of the Cenozoic on the speciation events in the Amazonian rainforest.

Some refuges have also been proposed for the Brazilian Atlantic Forest (e.g., Car-
naval and Moritz 2008, Carnaval et al. 2009), suggesting that these areas might have
indeed served as stable forest patches for many forest-dwelling taxa throughout climat-
ic-vegetational changes. Moreover, because each species has its own ecological niche,
idiosyncratic responses to alterations as well as different distribution of refuges are
expected for different species.

Richards (1978) considered that climatic-vegetational changes could have affected
the distribution of species but pointed out that paper wasps had not showed clear evi-
dence for refuge areas. Indeed, there are no empirical data concerning this matter, but
distribution of some species denote that the retraction of South American rainforests
during dry periods disrupted populations of Epipona media Cooper, Synoeca septen-
trionalis Richards and Angiopolybia pallens (Lepeletier) (Menezes et al. 2010, 2011,
Carvalho et al. 2014).

Phylogeographic analyses carried out with the extinction-threatened ant Dinopon-
era lucida Emery (Resende et al. 2010) and with orchid bees (Lopez-Uribe et al. 2014)
indicated that, in fact, different size refuges were important for the creation and main-
tenance of hymenopterans’ diversity in the Neotropical rainforests. For paper wasps,
however, there are no studies on this matter.

Paleogeography and River hypotheses

According to these hypotheses, different models are expected to have caused geo-
graphic separation and speciation of the animal populations in the Amazonian rain-
forest that are related to worldwide sea level changes, uplifts of plateaus and flooding
of plains. The emergence of islands (Island Model (Emsley 1965, Croizat 1976)),
archs (Arch Model (Morell 1996)), lagoons (Lagoon Model (Marroig and Cerqueira
1997)) and rivers (River hypothesis (Sick 1967)) in the Amazonian basin were recog-

Polistinae biogeography in the Neotropics: history and prospects 99

nized as historical events that putatively shifted species’ distribution ranges, facilitat-
ing their differentiation.

Despite Haffer (2008) arguing that some of these inferences are highly speculative
and contain several missing links, it is possible that such alterations in the geography
of the Amazonian region, if they occurred during the Cenozoic, would have provided
a great variety of environments for diversification of paper wasps. Furthermore, it is
not surprising that large bodies of water might act as barriers to the flow between
disrupted populations of land species. For wasps, that would not be different. Indeed,
swarms have great difficulty in dispersing across water (Jeanne 1981). This fact possibly
affected the decline of paper wasps in the Caribbean, for example, due to limitations of
the chemical trail system, but might not be a very convincing overall explanation since
the subfamily is present throughout Southeast Asia, the Philippines, and Australia
(Carpenter and Grimaldi 1997), for example.

Mainland species in turn might also have had their distributions altered during
landscape changes in the Cenozoic caused by both water barriers and tectonic events.
As showed by Silva and Noll (2014), phylogenetics and distribution data call atten-
tion to the importance of land bridges connecting the Northern and Southern Hemi-
spheres to the cladogenesis of basal species of genus Brachygastra Perty. Unfortunately,
although these alterations have influenced substantially the distribution of some land
organisms (Croizat 1976, Hershkovitz 1977), it is not possible to our knowledge to
quantify precisely how much these changes have contributed to extinction, disruptions
and speciation events of paper wasps.

Disturbance-Vicariance hypothesis

This hypothesis regards the influence of cold/warm cycles (not dry/humid, as proposed
by the Refuge hypothesis) as selecting Amazonian lineages throughout temperature
oscillations during the Pleistocene (Colinvaux 1993, Bush 1994). Invasion, counter-
invasion and competitive interactions are seen in this model as events affecting dis-
tributions and abundances of species. According to these assumptions, the presence
of invading and cold-adapted taxa could have resulted in local extinctions, favoring
isolation of genotypes and allopatric speciation of some taxa.

There is a regional focus of this hypothesis on the peripheral areas of the Amazo-
nian rainforest due to the high faunal endemism in such areas. Such regions are recog-
nized by the model as being rich in endemic taxa due to their supposed environmental
instability. Indeed, temperature oscillations during the Pleistocene might have influ-
enced the distribution of taxa and genotypes, but speciation events are mostly expected
to have occurred before 1.8 Mya (Zink and Slowinski 1995, Costa 2003).

The Quaternary is undoubtedly a short time to explain the huge diversity of paper
wasp species in the Neotropics. Both temperature oscillations and the short period,
however, are apparently sufficient for population structuring mainly of widely dis-
rupted taxa. Polistinae species might have undergone their distribution to optimal lo-

100 Antonio E Carvalho et al. / Journal of Hymenoptera Research 42: 93-105 (2015)

cations during such changes in the temperature and environmentally related genotypes
might have been frequently selected. Such alterations might also have influenced both
behavioral and physiologic traits, including feeding habits, defense, nest building, re-
sistance to diseases and predators and adaptive strategies against cold or warm climate.
Future researches are undoubtedly needed for accurate detailing.

Future directions

Since ecological and phylogenetic information can comprise very useful frameworks
for raising hypotheses on historical biogeography in scenarios constantly in change,
to explore the different impact of variables on the distribution of Polistinae is an im-
portant subject to be discussed. Furthermore, the knowledge of environmental and
geological constraints that affect distribution of species can help predictions about
extrinsic mechanisms shifting large-scale distributional patterns. In addition, to resolve
important questions like the causes of some clades disperse to some areas but not to
others is the major challenge in historical biogeography (Wiens and Graham 2005)
and define the favorable and unfavorable conditions that unbalance population den-
sity over time figures as a crucial factor to describe distribution of any group (Haldane
1956). However, understanding how extrinsic factors alter distribution we can deter-
mine environmental and ecological constraints that species can tolerate or not and,
likewise, which regions these species might occupy by dispersal events.

A very promising group of paper wasps for start this kind of research is that com-
posed by forest-dwelling species. Using data regarding current distribution, one can
propose past and present distributions of acceptable conditions for a clade to occur,
based on ecological niche modelling, for example (e.g., Hugall et al. 2002, Carnaval
et al. 2009). Since the bioclimatic conditions that maintain the distribution of humid
forests have changed in the Neotropics during ice ages and since forest-dwelling species
depend on forest coverage to nest and forage, the distribution of these wasps has likely
responded in a convergent manner to these alterations. Thinking about the biogeo-
graphic research of paper wasps in the next years, the formulation of potential paleodis-
tribution models might be considered a cornerstone that will drive population genetics
hypotheses, mostly based on phylogeographic frameworks, in studies of these insects.

Specialized literature related to the distribution or phylogenetics is very common for
different clades of paper wasps. However, a fine-scale distribution pattern of Neotropical
Polistinae could be more precisely understood by reviewing specialized literature; i-e.,
species by species. Also, tests of hypotheses using these data for making inferences about
the ecological and evolutionary causes of the success or failure of Polistinae in colonizing
certain regions have been rarely done. For example, the Tropical Niche Conservatism
hypothesis (Wiens and Graham 2005) could explain the tendency of paper wasps to
inhabit tropical areas instead of temperate regions since the subfamily was originated
in a similar environment (i.e., tropical Asia). A strategy for testing such a hypothesis
could be based on the integration of physiological responses, such as thermoregulation,

Polistinae biogeography in the Neotropics: history and prospects 101

and population relationships in the study of dry-adapted lineages of paper wasps. Since
niche conservatism predicts that unaltered lineages are not likely to habit areas character-
ized by conditions different from fundamental niches, lineages of a clade showing ther-
moregulatory responses different from their ancestral populations would be expected to
be adapted to local climatic alterations as a result of niche expansion.

Many recent studies have shown that integrative approaches linking climatic and
phylogeny-based information to explain biogeographical patterns might be very useful
for testing explicit hypotheses of causation by particular, mostly environmental, events
(Hugall et al. 2002, Waltari et al. 2007, Carnaval et al. 2009). Moreover, recent discus-
sions have drawn attention to the strong connection between evolutionary processes
(e.g., ecological specialization) and environmental events such as climatic-vegetational
changes in shaping the distribution of organisms over time (Wiens 2004, Hoorn et al.
2010). Quantifying the different impacts of each of these factors in the evolutionary
history of Polistinae should be regarded as the main challenge in the future of biogeog-
raphy and speciation research of the subfamily. The study of biogeographical processes
using such wasps as models can also aid in our understanding of significant events
that have influenced the distribution, historical demography and extinctions of the
Neotropical biota, including the disjunction between Amazonia and Atlantic Forest
and the demographic retraction of populations adapted to rainforest conditions during
glacial periods, for example.

Despite Ezenwa et al. (1998) have proposed possible periods for the arising of the
Polistinae tribes, current techniques are more precise for inferring divergence times.
Based on a molecular clock model, which permits dating putative splits between line-
ages using fossil-calibrated phylogenetic trees, the proposal of the geological periods
in which the subfamily Polistinae and its four tribes arose, as well as temporal concen-
tration of speciation events, would be more convincing. Such research could also be
conducted to test hypotheses regarding the influence of geological events such as river
formation and land uplifts on the separation of lineages since the periods in which
these events occurred are known.

In light of the differences regarding life histories, occupied niches, huge diversity,
etc., the Neotropical paper wasps represent an interesting group to be used as model in a
wide range of studies. However, biogeographic patterns as colonization routes and causes
behind alterations on the distribution have not been sufficiently discussed using advanced
analyses. We expect that by focusing on some of the challenges presented in this work, the
study of biogeography with these wasps will progress in the forthcoming years.

Acknowledgements

This study was supported by Fundacao de Amparo a Pesquisa do Estado de Sao Paulo
(FAPESP, 2011/13391-2 and BEPE 2013/04317-9) through a Ph.D. scholarship for
the first author. Our most sincere thanks are addressed to Ana Carolina Carnaval (The

City University of New York, USA), Fernando Noll and Marjorie Silva (UNESP, Sao

102 Antonio FE. Carvalho et al. / Journal of Hymenoptera Research 42: 93-105 (2015)

José do Rio Preto, Brazil), Gilberto Santos (UEFS, Feira de Santana, Brazil), Reinaldo
Brito and Evandro Moraes (UFSCar, Sao Carlos, Brazil) and one anonymous reviewer,
whose commentaries improved the manuscript.

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