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'Proximate Causes of Rensch's Rule: Does Sexual Size Dimorphism In Blanckenhorn, W U; Dixon, A F G; Fairbairn, D J; Foellmer, M W; Gibert, P; van der Linde, K; Meier, R; Nylin, S; Pitnick, S; Schoff, C; Signorelli, M; Teder, T; Wiklund, C (2007). Proximate Causes of Rensch's Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time? The American Naturalist, 169(2):245-257. Postprint available at: University of Zurich http://www.zora.uzh.ch Zurich Open Repository and Archive Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch Originally published at: Winterthurerstr. 190 The American Naturalist 2007, 169(2):245-257. CH-8057 Zurich http://www.zora.uzh.ch Year: 2007 Proximate Causes of Rensch's Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time? Blanckenhorn, W U; Dixon, A F G; Fairbairn, D J; Foellmer, M W; Gibert, P; van der Linde, K; Meier, R; Nylin, S; Pitnick, S; Schoff, C; Signorelli, M; Teder, T; Wiklund, C Blanckenhorn, W U; Dixon, A F G; Fairbairn, D J; Foellmer, M W; Gibert, P; van der Linde, K; Meier, R; Nylin, S; Pitnick, S; Schoff, C; Signorelli, M; Teder, T; Wiklund, C (2007). Proximate Causes of Rensch's Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time? The American Naturalist, 169(2):245-257. Postprint available at: http://www.zora.uzh.ch Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch Originally published at: The American Naturalist 2007, 169(2):245-257. Proximate Causes of Rensch's Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time? Abstract A prominent interspecific pattern of sexual size dimorphism (SSD) is Rensch's rule, according to which male body size is more variable or evolutionarily divergent than female body size. Assuming equal growth rates of males and females, SSD would be entirely mediated, and Rensch's rule proximately caused, by sexual differences in development times, or sexual bimaturism (SBM), with the larger sex developing for a proportionately longer time. Only a subset of the seven arthropod groups investigated in this study exhibits Rensch's rule. Furthermore, we found only a weak positive relationship between SSD and SBM overall, suggesting that growth rate differences between the sexes are more important than development time differences in proximately mediating SSD in a wide but by no means comprehensive range of arthropod taxa. Except when protandry is of selective advantage (as in many butterflies, Hymenoptera, and spiders), male development time was equal to (in water striders and beetles) or even longer than (in drosophilid and sepsid flies) that of females. Because all taxa show female-biased SSD, this implies faster growth of females in general, a pattern markedly different from that of primates and birds (analyzed here for comparison). We discuss three potential explanations for this pattern based on life-history trade-offs and sexual selection. vol. 169, no. 2 the american naturalist february 2007 ൴ Proximate Causes of Rensch’s Rule: Does Sexual Size Dimorphism in Arthropods Result from Sex Differences in Development Time? Wolf U. Blanckenhorn,1,* Anthony F. G. Dixon,2,† Daphne J. Fairbairn,3,‡ Matthias W. Foellmer,4,§ Patricia Gibert,5,k Kim van der Linde,6,# Rudolf Meier,7,** So¨ren Nylin,8,†† Scott Pitnick,9,‡‡ Christopher Schoff,9 Martino Signorelli,1 Tiit Teder,10,§§ and Christer Wiklund8,kk 1. Zoologisches Museum, Universita¨t Zu¨rich-Irchel, suming equal growth rates of males and females, SSD would be Winterthurerstrasse 190, CH-8057 Zu¨rich, Switzerland; entirely mediated, and Rensch’s rule proximately caused, by sexual 2. School of Biological Sciences, University of East Anglia, differences in development times, or sexual bimaturism (SBM), with Norwich NR4 7TJ, United Kingdom; the larger sex developing for a proportionately longer time. Only a 3. Department of Biology, University of California, Riverside, subset of the seven arthropod groups investigated in this study ex- California 92521; hibits Rensch’s rule. Furthermore, we found only a weak positive 4. Department of Biology, St. Mary’s University, 923 Robie Street, relationship between SSD and SBM overall, suggesting that growth Halifax, Nova Scotia B3H 3C3, Canada; rate differences between the sexes are more important than devel- 5. Laboratoire Biometrie et Biologie Evolutive, Universite´ Claude opment time differences in proximately mediating SSD in a wide Bernard Lyon 1, 43 Boulevard du 11 novembre 1918, F-69622 but by no means comprehensive range of arthropod taxa. Except Villeurbanne, France; when protandry is of selective advantage (as in many butterflies, 6. Sections of Animal Ecology and Evolutionary Biology, Institute Hymenoptera, and spiders), male development time was equal to (in of Biology, Leiden University, P.O. Box 9516, NL-2300 RA Leiden, water striders and beetles) or even longer than (in drosophilid and The Netherlands; sepsid flies) that of females. Because all taxa show female-biased SSD, 7. Department of Entomology, Zoological Museum, this implies faster growth of females in general, a pattern markedly Universitetsparken 15, DK-2100 Copenhagen, Denmark; and different from that of primates and birds (analyzed here for com- Department of Biological Sciences, National University of parison). We discuss three potential explanations for this pattern Singapore, 14 Science Drive 4, Singapore 117543, Republic of based on life-history trade-offs and sexual selection. Singapore; Keywords: allometry, body size, development time, gonads, growth, 8. Department of Zoology, Stockholm University, S-106 91 Rensch’s rule, sexual size dimorphism, sexual selection. Stockholm, Sweden; 9. Biology Department, Syracuse University, Syracuse, New York 13244; 10. Institute of Botany and Ecology, University of Tartu, Lai 40, Sexual size dimorphism (SSD) is widespread in the animal EE-51005 Tartu, Estonia kingdom (Hedrick and Temeles 1989; Shine 1989; Fair- bairn 1997). In most ectotherms, females are larger than Submitted March 22, 2006; Accepted August 28, 2006; males (Arak 1988; Shine 1988, 1989; Fairbairn 1997), Electronically published December 20, 2006 whereas in many birds and mammals, males are larger (Ralls 1977; Cabana et al. 1982; Abouheif and Fairbairn Online enhancement: appendix table. ‡ E-mail: [email protected]. § E-mail: [email protected]. k E-mail: [email protected]. abstract: A prominent interspecific pattern of sexual size dimor- # Present address: Department of Biological Science, Florida State University, phism (SSD) is Rensch’s rule, according to which male body size is Tallahassee, Florida 32306; e-mail: [email protected]. more variable or evolutionarily divergent than female body size. As- ** E-mail: [email protected]. †† * Corresponding author; e-mail: [email protected]. E-mail: [email protected]. ‡‡ † E-mail: [email protected]. E-mail: [email protected]. §§ Am. Nat. 2007. Vol. 169, pp. 245–257. ᭧ 2007 by The University of Chicago. E-mail: [email protected]. 0003-0147/2007/16902-41714$15.00. All rights reserved. kk E-mail: [email protected]. 246 The American Naturalist 1997; Sze´kely et al. 2000, 2004). However, beyond these nutrient-limited environments (Gotthard et al. 1994; broad generalizations, the direction and degree of SSD is Blanckenhorn 1998). Body size, development time, and highly variable within and between taxa. Rensch (1950) growth rate are thus intimately interconnected and traded observed that SSD increases with body size in species where off against each other, and they should therefore be in- males are larger and decreases with body size in species vestigated in conjunction (Nylin and Gotthard 1998). where females are larger (recently termed Rensch’s rule; Presuming no intraspecific sex difference in egg size, Abouheif and Fairbairn 1997; Fairbairn 1997). This is for which there is generally no evidence in arthropods (e.g., equivalent to saying that male body size varies or diverges Yasuda and Dixon 2002), the SSD of any given species more over evolutionary time than female body size, ir- may consequently be proximately caused by differences respective of which sex is larger. While Rensch (1950) did between the sexes in development time and/or growth rate. not offer an explanation for this phenomenon, Fairbairn There is substantial evidence in a number of taxa that both and Preziosi (1994) were the first to hypothesize that sexual growth rate and development time can vary between the selection for large male size may be the primary force sexes and that this variation is associated with SSD (Wik- driving this allometric pattern in SSD. Since then, some lund and Fagerstro¨m 1977; Wiklund et al. 1991; Leigh additional evidence for this hypothesis has been published 1992; Shine 1994; Teather and Weatherhead 1994; Badyaev (Abouheif and Fairbairn 1997; Fairbairn 1997; Sze´kely et et al. 2001a, 2001b). Leigh (1992) investigated the ontog- al. 2000, 2004; Kraushaar and Blanckenhorn 2002; Lin- eny of SSD in anthropoid primates and found that sex denfors et al. 2003), but more studies are clearly needed differences in both growth rate and age at maturity con- (Fairbairn 1997). tribute to SSD. In insects, the relationship between de- Rensch’s rule thus refers to a systematic pattern of in- velopment time and SSD has been discussed either in the terspecific (and sometimes, by extension, analogous in- context of protandry, that is, earlier male emergence (Wik- traspecific, between-population) variation in SSD (e.g., lund and Fagerstro¨m 1977; Fagerstro¨m and Wiklund Fairbairn and Preziosi 1994). For any particular species, 1982), or in the context of developmental constraints, the which sex is larger depends on whether selection for (pri- constraint being the presumed strong correlation (or marily fecundity selection in females and sexual selection trade-off) between body size and development time men- in males) and against (primarily viability selection) large tioned above (Roff 1980, 1992; Wiklund and Karlsson body size equilibrate differently in the two sexes (the so- 1988; Fairbairn 1990).
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