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 biogeography, mostly in the integration of ecological and evolutionary information, we highlight directions for future biogeographical research within the group.

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

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 colonization routes, population genetics and phylogeography have not been featured in discussions of paper wasps’ biology, thereby seriously limiting our ability to draw evolutionary 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; Maldonado-Coelho 2012), ants (Resende et al. 2010) and plants (Pinheiro et al. 2013). Also, population relationships and historical demography are unknown for the subfamily 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 environmental conditions (e.g., Dejean et al. 2011). In addition, the historical reasons regarding 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 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.

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 Gondwanan.” 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 important event in the evolutionary history of the group. Carpenter (1996) also reviewed the two main hypotheses of Polistinae biogeography and performed Component Analyses 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 reviewed some of these studies, focusing on paleontological, phylogenetic and divergence time evidence.

Distinct from other regions of the globe, the Neotropics are composed of large, humid 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 environmental changes and hypotheses regarding extrinsic processes (non-genetic mechanisms) 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 climatic phenomena such as El Niño and La Niña 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 processes 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.

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 important 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 density over time figures as a crucial factor to describe distribution of any group (Haldane 1956). However, understanding how extrinsic factors alter distribution we can determine 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 composed 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 biogeographic research of paper wasps in the next years, the formulation of potential paleodistribution 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, 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 characterized by conditions different from fundamental niches, lineages of a clade showing thermoregulatory 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 discussions 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 biogeography 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 lineages 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 concentration 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.

This study was supported by Fundação de Amparo à Pesquisa do Estado de São 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, São José do Rio Preto, Brazil), Gilberto Santos (UEFS, Feira de Santana, Brazil), Reinaldo Brito and Evandro Moraes (UFSCar, São Carlos, Brazil) and one anonymous reviewer, whose commentaries improved the manuscript.