Head-to-body size allometry in (): does brain housing constrain the evolution of small body sizes?

S. O’Donnell

Insectes Sociaux International Journal for the Study of Social

ISSN 0020-1812 Volume 66 Number 4

Insect. Soc. (2019) 66:647-651 DOI 10.1007/s00040-019-00715-x

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Insectes Sociaux (2019) 66:647–651 https://doi.org/10.1007/s00040-019-00715-x Insectes Sociaux

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Head‑to‑body size allometry in wasps (Vespidae): does brain housing constrain the evolution of small body sizes?

S. O’Donnell1

Received: 17 March 2019 / Revised: 24 June 2019 / Accepted: 27 June 2019 / Published online: 3 July 2019 © International Union for the Study of Social Insects (IUSSI) 2019

Abstract Species of wasps in the Vespidae family range widely in body size. Vespid species’ mean brain size increases relative to head capsule size in smaller species. In this study, I tested whether head capsule size varied allometrically with overall body size. I compared species ranging in body size from some of the largest to the smallest species. I found that relative head capsule volume and weight showed negative allometry with body size: relative head size was larger in smaller species. This signifcant negative relationship held after accounting for phylogenetic efects, and the negative allometry held when only social species were analyzed. I suggest that limits on minimum brain size have afected the evolution of body allometry in vespid wasps. Negative head-to-body allometry may be caused by the need to accommodate relatively large brains in smaller bodied species, and brain-driven needs for allometrically enlarged heads could place lower limits on body size evolution in the Vespidae. The relatively large brains of small species could afect head capsule cuticle thickness or muscle mass, with biomechanical implications for species’ behavior and ecology.

Keywords Biomechanics · Brain evolution · Constraints · Haller’s rule · Independent contrasts ·

Introduction evolution of allometric changes in head-to-body trunk (tho- rax plus abdomen) ratios as smaller body sizes evolved. Reproductive caste-related diferences in body size and The distributions of relative brain sizes can vary among shape are well-known for females in the social yellow- clades, but within clades, Haller’s rule generally jackets and hornets (Vespinae) and for some paper wasps applies: smaller species have larger relative brain sizes (Roth (Polistinae) (O’Donnell 1998; Noll et al. 2004; Kovacs et al. et al. 1990; Eberhard and Wcislo 2011; Quesada et al. 2011; 2010; Perrard et al. 2012). However, species diferences in Seid et al 2011; Ocampo et al. 2018). Comparative studies of the proportions of body regions are relatively poorly known size-related brain allometry among social Vespidae species in Vespidae. Wasps in this family vary widely in body size. supported Haller’s rule: the ratio of brain size to body size Because all Vespidae can fy, aerodynamic considerations increased with decreasing species’ head size (O’Donnell and such as drag and weight distribution are expected to impose Bulova 2017; O’Donnell et al. 2018). In the smallest wasp constraints on body allometry, particularly when wasps are species sampled, brain volume comprised approximately compared to social insects with walking workers such as 12% of head capsule volume, compared to brains occupy- ants and termites (Dudley 2002). Despite the expected bio- ing approximately 2% of head capsule volume in the largest mechanical constraints on wasp allometry, I present data species. suggesting there is signifcant body size-related allometry Increases in relative brain size are associated with body of head capsule size among species of Vespidae. I propose modifcations in the smallest species of diverse animal taxa that brain size-related selective pressures have driven the (Hanken 1983, 1984; Polilov 2015). Not surprisingly, heads and other body regions that house brains (e.g., the cephalo- thorax in spiders) are especially subject to modifcation. Are * S. O’Donnell head capsule volumes a good indicator of overall body size [email protected] in Vespidae, as predicted under head–body isometry? Or, do wasp head capsules vary allometrically with body size 1 Biodiversity Earth and Environmental Science, Drexel in this family? I collected data on dry weights of the main University, Philadelphia, PA 19104, USA

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648 S. O’Donnell trunk of the body (the thorax and abdomen) for the vespid Polybia dimidiata, Polybia richardsi, Protopolybia exigua, wasp species that were sampled for brain size and head cap- septentrionalis: June 2007, Ecuador, 0°40.3′S, sule volumes (O’Donnell et al. 2018), and I measured dry 76°24.0′W; Polybia favitincta (n = 3): March 2012, Costa weights for bodies and head capsules of additional species. Rica: 10°25.6′N, 84°1.2′W Brachygastra smithii, Polybia I asked whether head capsule size, indicated by both volume aequatorialis, Polybia plebeja, Polybia rejecta: July 2012, and by weight, varied allometrically with body trunk weight. 10°16.3′N, 84°49.4′W.

Methods Head capsule volumes

Taxon sampling Head capsule volumes were calculated from digital photo- graphs (O’Donnell et al. 2018). I dissected the wasp’s head capsules from the body at the foramen or “neck” (the narrow I sampled social species from all four tribes of the subfamily attachment point to the alitrunk) and photographed them Polistinae (Piekarski et al. 2018): two independent-founding using a digital camera mounted on a dissecting scope. Heads Ropalidiini, one independent-founding Mischocyttarini, were photographed in frontal view with the foramen area three independent-founding Polistini, and 21 swarm-found- facing away from the camera and resting against a horizontal ing . I also sampled four species of the subfamily glass surface. I used the ruler tool in ImageJ and photographs Vespinae and fve species of solitary-nesting potter wasps of a stage micrometer taken at the same magnifcation on the (subfamily Eumeninae) for a total of n = 36 subject species. same scope to convert pixels to mm. I measured head width All subject individuals were mature females; in most cases, at the widest point, head height from the ventral center edge the social wasps were workers collected outside or away of the clypeus to the vertex and used 1/2 head width as an from their nests, but in some cases, caste was not known. In approximation of head depth. I estimated head capsule vol- calculating species mean sizes, I assumed caste diferences ume for each wasp using the formula for an ellipsoid: in morphology would be small in magnitude relative to spe- cies diferences. 4∕3 × × 1∕2 head width (mm) × 1∕2 head height (mm) Unless noted otherwise below, I measured n = 5 heads and × 1∕2 head depth (mm). bodies to obtain the species mean values of head and body size for each subject species. Subject species, collection Head capsule and body trunk weights dates, and locations were: Solitary potter wasps, Eumeninae: Coeleumenes burmanicus n Delta esuriens n ( = 1), ( = 2), I measured dry weights of body parts for the subject species Delta pyriforme n Phimenes flavopictus n ( = 1), ( = 3), where specimens were available. I dissected wasps’ head Rhynchium quinquecinctum n ( = 2), May 2014, May 2014, capsules from the body trunk (thorax and abdomen) by cut- ′ ′ Vespa Taiwan: 21°57.8 N, 120°49.5 E. Social Vespinae: ting at the foramen (neck). Head capsules and bodies were ducalis n V. afnis n ( = 4) and ( = 1): May 2014, May 2014, dried separately to constant weight in a convection oven at ′ ′ Dolichovespula maculata Taiwan: 21°57.8 N, 120°49.5 E; : 50 °C. I weighted the body parts (head and trunk) separately September 2010, Seattle, WA USA, 47.659°N, 122.281°W; on a digital balance to the nearest 0.0001 g. I measured Vespula vidua : September, 1992, Madison, WI 43.07°N, body trunk weights for all subject species and head capsule Mischocyt- 89.41°W. Social Polistinae, Mischocyttarini: weights for n = 29 of the subject species. tarus mastigophorus, August 2006, Costa Rica, 10°18.1′N, 84°47.9′W. Social Polistinae, Polistini: Polistes aterrimus (n = 2): August 2006, Costa Rica, 10°14.4′N, 84°54.3′W; Statistical analyses P. instabilis: July 2005, Costa Rica, 10°27.2′N, 85°7.5′W; P. gigas, May 2014, Taiwan: 21°57.8′N, 120°49.5′E. Social Analyses were performed in SPSS software (version 24) Polistinae, Ropalidiini: varia, fas- and Sigmaplot (version 12.5) on species mean values of all ciata: May 2014, Taiwan: 21°57.8′N, 120°49.5′E. Social variables. Brain volumes, head capsule volumes, and body Polistinae, Epiponini: Apoica thoracica (n = 2): March 2009, weights were ­log10 transformed for analyses, except that Costa Rica, 8.785°N, 82.958°W; Polybia jurenei: November volume or weight ratios were not transformed. I used Phy- 1994, Ecuador, 0°40.5′S, 76°25.8′W; Agelaia xanthopus, A. locom version 4.2 software (Webb et al. 2008) to account panamaensis (n = 4), Polybia emaciate (n = 4): August 2006, for phylogenetic efects in the analysis of (head volume-to- Costa Rica, 10°18.1′N, 84°47.9′W; Nectarinella cham- body weight ratio) vs. body weight. I calculated independent pioni, Polybia raui: August 2006, Costa Rica, 10°14.4′N, contrasts with all branch lengths set to one (default setting). 84°54.3′W; Apoica pallens, Angiopolybia zischkai, Char- I tested for signifcance of the independent contrasts trait terginus fulvus, Leipomeles dorsata, Parachartergus smithii, correlation by consulting a signifcance table for Pearson

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Head-to-body size allometry in wasps (Vespidae): does brain housing constrain the evolution… 649 correlation coefcients. Phylogenetic relationships among species were obtained from Piekarski et al. (2018).

Results

The two measures of head size, head capsule volume, and head capsule weight were strongly positively correlated (Fig. 1; n = 24, r = 0.97, p < 0.001). By both measures, species-mean relative head sizes decreased with body size; in other words, smaller bodied species had relatively large heads as shown below.

Head volume allometry Fig. 2 Signifcant negative relationship between the species mean Species sampling was most complete for head capsule ratio of (head capsule volume/body trunk weight) with body trunk volume. The ratio of head capsule volume to body trunk weight for species of Vespidae (open circles: Polistinae; gray trian- weight (thorax and abdomen) decreased signifcantly with gles: Vespinae; black diamonds: Eumeninae) body trunk weight (Fig. 2; n = 32, r2 = 0.78, p < 0.0001). The highly signifcant negative correlation between (head Polistinae (n = 26, r2 = 0.37, p = 0.0009). The magnitude of volume-to-body weight ratio) and body trunk weight held variation in relative head size was substantial. Head weight after accounting for the efects of phylogeny (independent comprised approximately 5% of body weight in some of the contrasts, r = − 0.80, df = 28, p < 0.0001). The signifcant largest species, but increased to nearly 30% of body weight negative relationship also held when analyzing only the in some of the smallest species (Fig. 3). social Polistinae (n = 24, r2 = 0.58, p < 0.0001).

Head weight allometry Discussion

For the species, where head capsule weight was measured, The data I present here suggest a key aspect of the ratio of head capsule weight to total weight (head, tho- body architecture—relative head size—evolved to increase rax and abdomen) decreased signifcantly with total weight as body size decreased. The need to accommodate relatively (Fig. 3; n = 29, r2 = 0.55, p < 0.0001); this significant large brains likely played an important role in driving this negative relationship held when analyzing only the social allometric change. Changes in body morphology to accom- modate relatively large brains, particularly in the head

Fig. 3 Signifcant negative relationship between the species mean Fig. 1 Signifcant positive correlation of species mean head capsule ratio of (head capsule weight/total body weight) with total body volume and head capsule dry weight (log/log) for species of Vespidae weight for species of Vespidae (open circles: Polistinae; gray trian- (open circles: Polistinae; gray triangles: Vespinae) gles: Vespinae)

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650 S. O’Donnell region, are observed in the smallest species of several animal such as muscles and exocrine glands (Landolt and Akre lineages (Polilov 2015; Ocampo et al. 2018). The evolution 1979; Downing and Jeanne 1983), could decrease in rela- of head vs. body allometry in Vespidae is a compelling test tive size to accommodate the larger brains of the smallest case because vespid wasps are fying insects. Allometric species. Many of the larger muscles in the head capsule exert changes in the relative sizes of body regions, such as the biting force via the mandibles and decreases in muscle mass relative size of the head, are likely to be highly constrained could infuence resource harvesting and material manipula- by biomechanical considerations related to powered fight tion by paper wasps. Alternatively, decreases in the thick- (Harrison and Roberts 2000; Feuerbacher et al. 2003). ness of the head capsule exoskeleton could allow for greater I suggest that the evolution of relatively large wasp heads interior brain space: relatively thin skulls evolved conver- was driven by the need to accommodate the relatively large gently in miniaturized species of several vertebrate lineages brains of smaller species. Haller’s rule is well-represented (Hanken 1984; Yeh 2002; Ocampo et al. 2018), and thin in paper wasps: relative to head size, brain size was larger head capsule cuticles are a common feature of smaller bod- in smaller species (O’Donnell and Bulova 2017; O’Donnell ied insects (Polilov 2015). If cuticle thinning has occurred et al. 2018). One interpretation of this pattern is that there in the smallest Polistinae, it would likely also come at costs is a lineage-specifc minimum brain size; as smaller bodies in terms of strength of the head capsule. This could further evolve, brains cannot surpass their minimum size and rela- diminish the capacity for exerting strong biting forces via tive brain size increases. Why do brains have taxon-specifc the mandibles and increase the risk of bodily damage during minimum sizes? Although vespid wasps vary widely in body combat with natural enemies. size, even the smallest species are larger than many other Brain investment-driven limitations on internal and social insects (e.g., many ants: Seid et al. 2011; Muscedere cuticular head capsule structure may afect the evolutionary et al. 2014), and vespid wasps likely do not confront the ecology of paper wasps. I hypothesize that reductions in neuronal and body-plan challenges that apply in extremely head musculature and possibly head cuticle thickness have miniaturized insects (Eberhard and Wcislo 2011; Niven and afected the behavior and ecology of the smallest bodied Farris 2012). The cognitive implications of reduced brain paper wasps. Some small-bodied species collect relatively size are difcult to predict across taxa (Gonzalez-Voyer et al. soft or pliable materials for nest construction, such as plant 2009; Eberhard and Wcislo 2011). Nevertheless, the basic hairs (Sarmiento 2004) or mud (Richards 1978). Whether behavioral and ecological repertoire of species in a clade paper wasp prey capture and processing (Raveret Richter such as Vespidae may require some minimum amount of 2000) have been afected by the evolution of head capsule brain tissue investment to support clade-typical cognitive anatomy and morphology is unknown. The anatomical and requirements. For example, processing and integration of biomechanical challenges imposed by relatively high invest- visual and olfactory sensory inputs by the brain are likely ment in brains may place limits on the evolution of reduced critical for achieving directed powered fight. body size in paper wasps, as has been suggested for other There are two potentially important implications of the taxa (Beutel et al. 2005; Grebennikov 2008). In insects, par- evolution of relatively large heads in Vespidae. The frst ticularly in the order , brain and reproductive is biomechanical. Vespid wasps are fying ; even system sizes may be the most important factors in setting queens in mature colonies maintain the capacity for powered lower limits on body size evolution (Polilov and Makarova fight, possibly favored by the need to abscond in response 2017). to predator attack or otherwise deteriorating nest conditions (West-Eberhard 1982). Increased body volume and weight at Acknowledgements Meghan Barrett, Susan Bulova, Sara Deleon, and Katherine Fiocca assisted with morphological data collection. Research the anterior end alter air fow and the center of gravity, which was funded by NSF grant 1209072 and the Drexel College of Arts and could impact fight stability for large-headed species (Har- Sciences. William Wcislo and an anonymous reviewer made valuable rison and Roberts 2000; Feuerbacher et al. 2003) and this comments on an earlier version of this paper. may set lower limits on vespid wasp body size. The second implication relates to brain size and Haller’s rule. Although head size increases relative to body size in smaller species, brain size relative to head size also increases in smaller spe- References cies. 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