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2012. The Journal ofArachnology 40:345-347 SHORT COMMUNICATION Nephila female gigantism attained through post-maturity molting Matjaz Kuntner''-'-^, Shichang Zhang'*, Matjaz Gregoric' and Daiqin ‘Institute ofBiology, Scientific Research Centre, Slovenian Academy of Sciences and Arts, Ljubljana, Slovenia. E-mail: [email protected]; -Department of Entomology, National Museum ofNatural History, Smithsonian Institution, Washington, D.C., USA; ’College ofLife Science, Hubei University, Wuhan 430062, Hubei, China; '‘Department of Biological Sciences, National University of Singapore, Singapore Abstract. Nephilaare known for thegreatest degrees ofsexual sizedimorphism amongorbweaving spiders (Araneoidea) and thus amongterrestrial animals. However, a meaningful quantification ofthedimorphism is lackingand the proximate developmental mechanisms of female gigantism are poorly understood, being attributed solely to female delayed maturation. Here we show that females in the giant wood spider Nephilapilipes (Fabricius 1793) become giants through facultative post-maturity molting, a phenomenon resulting in female carapaces on average 4.27 times longer than males’ (rangingfrom 3 to6.4times), and femalemassaveraging 125 timesthemale’s(rangingfrom 28 to 502times). Although the small malesfollowatypical-developmentalpathwayand reach maturitywith theirfinal molt, thefemalesmatureatvarying sizes and instars and then continue to grow by molting the entire exoskeleton except their genitals. The newly discovered phenomenon ofadditional, single-sex, adult, non-genital molting may represent a critical developmental adaptation that facilitates female gigantism in Nephila as a response to fecundity selection. Keywords: Sexual size dimorphism, development, fecundity selection, spider, Nephilapilipes Sexual size dimorphism (SSD) describes a morphological syndrome laboratory, we reared the males in plastic cups and the subadult in which male and female sizes differ significantly within a species. and adultfemalesin theirownwebsmadein frames. Wefed themales Although well-known vertebratecasesexist wheremalesarethe larger fruit (lies, and the females Hies and mealworms thrice a week, and sex, moredramaticsexual sizedifferencesare usuallyfound inanimals watered them daily. with female-biased SSD (Norman et al. 2002). A variety ofselection In mostspidersmoltingceaseswith maturity,and thishasalsobeen pressures may account for the evolution of female-biased SSD; a conventionally presumed in Nephila and other araneoid spiders (for commonlyinvokedexplanationisfecundityselection,whichpostulates exceptions, see below). However, in our pool of40 subadult females that increased female size enables greater egg production (Higgins that were subjected to daily monitoring until their maturity, 27 2002; Kuntner & Coddington 2009). However, in arthropods, (67.5%) molted even after maturity (mean number ofmolts = 1.15, evolution towards gigantic females acts against substantial develop- range = 1-2; SD = 0.36, n = 27). Our morphological examination of mental constraints, as arthropods can only grow by molting, which 17 molts(orexuvia) that were shed aftermaturity revealed no molted almost invariably ceases upon maturity (e.g., Stillwell & Davidowitz genital structures. Each exuvium contained a hole in the part of the 2010; Foelix 2011). ventral abdomen thatcontains thegenitals (Fig. lb). No adult female Among terrestrial animals, the most extreme female gigantism is molted after egg sac and plug formation (Kuntner et al. 2012). found in orb weaving spiders, clade Araneoidea (Foellmer & Moya- Adult female carapace length ranged between 7.09 and 11.52 mm aLraeranpoost2u0l0a7t)e.d,AtalneadsttfhoeusreinadreepenpdreendtompihnyalnotgleynetciacseosrigoifnsfoefmSalSeDs (bemtewaenen=18..8800amnmd,2S.3D6 =mm0.9(0mmeamn,=« =2.0361)m, man,dSthDat=of0.m1a5lemsmr,annge=d becoming evolutionary giants (Hormiga et al. 2000). Classical cases 50). Adult femalesweighed between 0.385 and 1.757g(mean = 0.930, of female gigantism have been reported in the family Nephilidae SD = 0.375, n = 31), and adult males between 0.0035 and 0.0137 g (Kuntner et al. 2008; Kuntner & Coddington 2009), in particular in (mean = 0.0074, SD = 0.002, n = 98). In our population, females thegenusNephila(Fig. la), although precisequantificationsofsexual were on average 4.27 times larger than males in carapace length mass differences are mostly lacking. In addition, the proximate (ranging from 3 to 6.4), but were 125 times heavier than the males mechanisms ofthe developmental pathways responsible for extreme (withextremes rangingfrom28 to 502timesmalemass). Accordingto female gigantism are not well understood and mostly attributed to the review ofFoellmer & Moya-Larano (2007), our SSD quantifica- delayed maturation in females as a response to fecundity selection tion in N. pilipesreflects the most extreme mass dimorphism reported (Higgins & Goodnight 2010; Higgins et al. 201 1). As most reports of in a terrestrial animal (for an extreme among marine animals, SSD in spiders derive from scattered measurements of body length, however, see Norman et al. 2002). and as body size is confounded with condition (Foellmer & Moya- Post-maturitymoltingwasmorelikelyin femalesthatcopulated for Larano 2007), body mass should instead serve as a bettermeasure of a shorter total duration (Mann-Whitney L = 81.5, « = 39, /* = SSD. Here, we report the range of female to male mass ratio as an 0.023), and, albeit non-significant, such a trend was also present in accurate quantification of female gigantism and compare it to the females exposed to lower levels of polyandry and fewer copulatory carapace size ratio. In addition we report our discovery of a insertions (Mann-Whitney U = 100, ii = 39, P = 0.088; number of previously unknown developmental mechanism that underlies female males: jp = 7.12, df = 3, P = 0.068). This suggests that females, gigantism in the giant wood spider Nephila pilipes (Fabricius 1793) regardless of their size and mass, may terminate their growth after (Fig. la). possessingenough sperm for oviposition, but that they may continue Wecollected 155 adult malesand 108 subadult femalesofN. pilipes to grow and molt if the number or duration of matings has been on Pulau Ubin, Singapore (1.421575°N, 103.932542°E). In the belowacertain threshold. It isimportant to note that moltingfemales 345 346 THE JOURNAL OF ARACHNOLOGY — Figure la, b. The giant wood spider Nepliilapilipes, a highly polygamous and sexually dimorphic species whose females are on average 125 times heavier than males, a. A gravid and fully grown female in nature supporting on her body a conspecific male and six kleptoparasitic flies, b. Female adult molt containing the entire abdominal exoskeleton except the genital area (arrow). do not shed their genitals and thus may retain sperm already stored. lay fertile eggs post molting. However, the rarity of post-maturity Such developmental plasticity may be a critical response to fecundity molting in Latrodeetiis, albeit suggestive of a potentially more selection, which in Nephiki results in extreme female gigantism. As widespread abilityofaraneomorph spideradults tomolt, nevertheless reported here, females are freed from developmental constraints to be suggeststhat itisnotan obligate, but ratheran anomalouslifehistory capable of growth beyond maturity and presumably increased egg trait (Kaston 1968). production. Other explanations are possible, however. For example, Because other araneoid spiders do not usually molt as adults, the chemical signaling by a molted female may attract more males, which mechanism of non-genital molting of adult Nephiki females may may serve the female as she strives for polyandry (Kuntner et al. repre.sent a critical developmental adaptation facilitating gigantism, 2012). In support of this may be the case oi' Nepliila clavata, where and involves the additional dimension of sexual dimorphism. males are highly attracted to recently molted females (Miyashita & Although N. piiipes males follow typical spider developmental Hayashi 1996). pathways and reach maturity with their final molt, females mature Our discovery ofpost-maturity female growth in Nephikipiiipes is at varying sizes and then continue to grow by molting the entire at odds with the conventional wisdom that most spiders exhibit exoskeleton except their genitals. However, it remains to be determinant growth and do not molt after maturity (Foelix 2011). established how typical such development is for Nephiki, or even if Post-maturity molting has predominantly been known in phyloge- it is prevalent in all populations of N. piiipes, a widespread species netically more ancestral and sexually monomorphic spiders such as ranging throughout South, Southeast and East Asia into Australasia liphistiids(Haupt 2003; Foelix2011)and mygalomorphs(Baerg 1958; (Su et al. 2007), and thus from rain forests to dry subtropical forests. Miyashita 1992; Schmidt 1993); in these groups oflong lived spiders, Post-maturity molting was apparently unknown to Harvey et al. adult female molting involves growth by shedding the entire (2007), who revised Australasian Nephiki. In their detailed studies of exoskeleton, including the genitals (Schmidt 1993; Foelix 2011). the Papuan population of N. piiipes (as N. maciikita), Robinson & However, studies havealso outlined casesofpost-maturity moltingin Robinson (1973, 1976) postulated 14instarsin the femaleand 7 in the phylogenetically scattered examples ofaraneomorph spiders, such as male. Theyacknowledged someconfusionastothenumberofinstars, social eresids, genus Stegodypim.s (Kraus and Kraus 1988), female but nevertheless only considered the last, 14”’ instar, to represent an filistatids (Vetter 2011) and male Lo.\osceles\ where, apparently, adult female. Similarly, in a developmental study, Higgins (2002) did eunuch males engage in fatal post-maturity molting attempts (Vetter not report that several large instars in females from Papua might 201 1). Thereexist someotherreportsforaraneomorphs, but most are represent adult, not subadult females, although she concluded that exceptional oranomalous (Fuji! 2001; see also Kayashima 1981). For males only go through four and females through about 10 instars. In example, as the only known case of post-maturity molting in ourpriormatingstudyon theSingaporepopulation, wealso failed to araneoids, Kaston (1968) reports it happened in five out ofhundreds takethisintoaccount(Kuntneretal. 2009). Webelievethatinstars 12 of black widow females {Lalrodecliis nuietaiis and L. Iiesperiis), and to 14 in the study ofRobinson & Robinson (1976) represented adult those molts, as in Nephiki, did not contain any epigynal structures; females ofdifferent sizes, and that such plastic development will be molted femalesin factretained enoughsperm in theirspermathecaeto typical ofall populations ofN. piiipes. In fact, wepredict it also to be KUNTNER ET AL—POST-MATURITY MOLTING IN NEPHILA 347 the case in its sister species, the African N. constricta (Kuntner et al. Kraus, O. & M. Kraus. 1988. The genus Stegodyphus (Arachnida, 2008; Su et al. 2011), which shows an unprecedented range ofadult Araneae). Sibling species, species groups and parallel origin of female sizes (Higgins et al. 2011). social living. Verhandlungeii des Naturwissenschaften Vereins in Biology of the giant wood spider Nephila pilipes never ceases to Hamburg 30:151-254. excite, as it is now known to encompass thelargest documented mass Kuntner, M. & J.A. Coddington. 2009. Discovery of the largest differencebetweensexesamongterrestrialorganisms,withfemaleson orbweaving spider species: The evolution ofgigantism in Nephila. average 125 times heavier than males. Furthermore, a previously PLoS ONE 4(10):e7516. unstudied developmental mechanism of additional adult growth Kuntner, M., J.A. Coddington & G. Hormiga. 2008. Phylogeny of through molting exists, in addition to a plethora of behavioral extant nephilid orb-weaving spiders (Araneae, Nephilidae): testing adaptations arising through sexual selection that we believe are morphological and ethological homologies. Cladistics 24:147-217. connected with, if not determined by, extreme SSD (Kuntner et al. Kuntner, M., J.A. Coddington & J.M. Schneider. 2009a. Intersexual 2009a). Notable examples of such behaviors are extreme polygamy, arms race? Genital coevolution in nephilid spiders (Araneae, matingplugs, genital mutilation, mate binding (Kuntneret al. 2009b, Nephilidae). Evolution 63:1451-1463. 2012; Zhang et al. 2011) and the construction ofgiant asymmetrical Kuntner, M., M. Gregoric & D. Li. 2010. Mass predicts web webs (Kuntner et al. 2010). asymmetry in Nephila spiders. Naturwissenschaften 97:1097-1105. ACKNOWLEDGMENTS Kuntner, M., M. Gregoric, S. Zhang, S. Kralj-Fiser & D. Li. 2012. We thank Simona Kralj-Fiser for help with data analysis and wMhaetni,nghopwlugasndinwhpyo?lyPanLdorSouOsNgEian7t(s7:):Weh4i09c3h9 2s0ex10.produces them, bRyicthhaerdSlGorveeenniaenfoRresheealrpcwhitAhgelintceryatgurrea.ntTshiasndreaseRaarfcfhlewsasMususpepuormteodf Kuntner, M., S. Kralj-Fiser, J.M. Schneider & D. Li. 2009b. Mate pluggingviagenital mutilation in nephilid spiders: anevolutionary Biodiversity Research Fellowship to M. Kuntner and the grant from hypothesis. Journal ofZoology 277:257-266. the Singapore Ministry of Education (MOE) Academic Research Fund (AcRF) (R-154-000-435-112) to D. Li, and authorized by the Miyashita, K. 1992. Postembryonic development and life cycle of Atypus karschi Doenitz (Araneae: Atypidae). Acta Arachnologica Singapore National Parks (Permit nu. NP/RP9880-1) with the kind 41:177-186. assistance ofJeremy Woon. Miyashita, T. & H. Hayashi. 1996. 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