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Head-To-Body Size Allometry in Wasps (Vespidae): Does Brain Housing Constrain the Evolution of Small Body Sizes?

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Head-To-Body Size Allometry in Wasps (Vespidae): Does Brain Housing Constrain the Evolution of Small Body Sizes? Head-to-body size allometry in wasps (Vespidae): does brain housing constrain the evolution of small body sizes? S. O’Donnell Insectes Sociaux International Journal for the Study of Social Arthropods ISSN 0020-1812 Volume 66 Number 4 Insect. Soc. (2019) 66:647-651 DOI 10.1007/s00040-019-00715-x 1 23 Your article is protected by copyright and all rights are held exclusively by International Union for the Study of Social Insects (IUSSI). This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Insectes Sociaux (2019) 66:647–651 https://doi.org/10.1007/s00040-019-00715-x Insectes Sociaux SHORT COMMUNICATION 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 wasp 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 · Polistinae 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- animal 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 Vol.:(0123456789)1 3 Author's personal copy 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- Synoeca 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. Costa Rica 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 Epiponini. 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: Parapolybia varia, Ropalidia 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.
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