Journal of Fish Biology (2015) doi:10.1111/jfb.12704, available online at wileyonlinelibrary.com
BRIEF COMMUNICATION Sexual size dimorphism in anadromous brown trout Salmo trutta B. Jonsson* and N. Jonsson Norwegian Institute for Nature Research, Gaustadalléen 21, 0349 Oslo, Norway (Received 16 January 2014, Accepted 20 March 2015) Anadromous trout Salmo trutta exhibits sexual size dimorphism (SSD ); females were larger than males in populations where male mean total length (LT ) at maturity was below 49 cm and females were smaller than males when mean male LT was above 49 cm, the slope of the regression of female on male LT was 0⋅59. In streams with mean annual discharge below 41 m3 s−1 , flow added significantly to a model with SSD as the dependent variable and male mean LT at maturity as the first predictor variable. There was a slight increase in SSD with increasing latitude, which may result from an increase in male size with increasing latitude. © 2015 The Fisheries Society of the British Isles
Key words: allometry; latitudinal cline; length at maturity; water flow.
Sexual size dimorphism (SSD ) is common in animals (Hedrick & Temeles, 1989; Blankenhorn, 2005). Males are often larger than females in birds and mammals, whereas females are typically the larger sex in invertebrates and poikilothermic vertebrates such as fishes (Andersson, 1994; Hirst & Kiørboe, 2014). Large females may be favoured through natural selection because fecundity and reproductive success increase with increasing body size. Large males may be favoured both through natural and sexual selection (Darwin, 1871); through natural selection because milt production increases with body size (Jonsson & Jonsson, 2005) and large males may be superior competitors on the breeding grounds (Fleming et al., 1996); through sexual selection because large males may be favoured by females (Järvi, 1990; Jonsson & Jonsson, 2011). When not environmentally constrained, large males have access to more females and perform a higher number of spawnings than smaller conspecifics (Fleming et al., 1996). According to Rensch’s rule (Rensch, 1960), male body size varies more than female body size, and SSD typically increases with body size when males are largest, but decreases with increasing size when females are largest (Lengkeek et al., 2008; Lisle & Rowe, 2013). Thus, among conspecific populations, the slope usually is 1 for male-biased and 0⋅05) or ln Q (P > 0⋅05) as the first independent variable. The clinal increase of SSD with latitude appeared to be caused by an increase in male size towards the © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
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Table I. Streams with latitude, annual average flow, latitude and male and female mean total length (LT ) at maturity of Norwegian anadromous Salmo trutta, and reference to the study where the data were collected Location Tana Halselva Alta Skibotnelva Salangselva Hellemoelva Kobbelv Saltdalselva Beiarelva Ranaelva Vefsna Åbjøra Almåselva Mølleelva Norddalselva Skeitjørnbekken Vikabekken Børsethelva Råelva Hofstadelva Klefstadbekken Storelva Botna Herjåa Loddbekken Malma Bævra Eira Driva Istra Korsbrekkelva Ommedalselva Jostedøla Lærdalselva Aurlandselva Dyrvo Granvinselva Eio Ørbekken Imsa Langangselva Østeråbekken Allemanns-bekken
Latitude (∘ N) 70⋅22 70⋅02 69⋅58 69⋅23 68⋅52 67⋅48 67⋅37 67⋅07 67⋅02 66⋅20 65⋅50 65⋅04 64⋅28 64⋅28 64⋅28 64⋅28 64⋅28 63⋅32 63⋅32 63⋅30 63⋅26 63⋅26 63⋅20 63⋅20 63⋅20 63⋅20 63⋅02 62⋅40 62⋅39 62⋅33 62⋅07 61⋅44 61⋅23 61⋅07 60⋅54 60⋅37 60⋅32 60⋅22 58⋅59 58⋅53 58⋅30 58⋅30 58⋅23
Flow (m3 s−1 ) 167 5 73 15 23 7 26 55 40 83 137 19 0⋅49 0⋅18 1⋅24 0⋅15 0⋅27 0⋅11 0⋅11 0⋅21 0⋅17 0⋅24 0⋅16 0⋅92 0⋅16 0⋅27 14 15 68 4 9 70 70 39 39 1⋅00 3 44 0⋅35 5⋅1 0⋅30 0⋅10 0⋅05
Male LT (cm)
Female LT (cm)
46⋅5 41⋅7 42⋅5 42⋅8 47⋅1 52⋅0 35⋅0 61⋅9 44⋅8 48⋅6 41⋅9 44⋅5 41⋅3 33⋅5 37⋅7 43⋅9 35⋅5 36⋅3 35⋅3 38⋅2 35⋅2 36⋅9 36⋅6 52⋅7 36⋅7 47⋅6 30⋅6 44⋅2 52⋅3 52⋅1 45⋅8 46⋅4 59⋅7 54⋅7 75⋅8 42⋅0 41⋅2 41⋅3 36⋅7 35⋅7 33⋅7 24⋅7 25⋅4
39⋅9 47⋅1 44⋅1 50⋅1 51⋅8 49⋅0 45⋅1 56⋅6 45⋅1 46⋅8 46⋅0 42⋅9 41⋅9 36⋅2 42⋅3 42⋅8 38⋅8 36⋅1 40⋅2 40⋅8 39⋅7 37⋅0 42⋅7 53⋅3 43⋅0 53⋅2 45⋅9 43⋅2 45⋅4 50⋅7 47⋅4 51⋅4 52⋅3 52⋅3 63⋅7 44⋅9 44⋅5 41⋅0 42⋅4 43⋅8 38⋅8 30⋅7 34⋅0
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
Reference L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) Jensen (1968) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) Jonsson (1985) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) Jonsson et al. (2001) Jonsson et al. (2001)
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Table I. Continued Location Grefstadbekken Mørfjærbekken Sævlibekken Helldalselva Slimestad-bekken Vesbekken Dårøybekken Røyseland-bekken Audna
Latitude (∘ N) 58⋅22 58⋅22 58⋅22 58⋅19 58⋅17 58⋅12 58⋅07 58⋅06 58⋅05
Flow (m3 s−1 ) 0⋅04 0⋅18 0⋅05 0⋅25 0⋅43 0⋅36 0⋅13 0⋅08 22
Male LT (cm)
Female LT (cm)
29⋅1 29⋅8 19⋅9 24⋅4 30⋅7 28⋅6 29⋅9 28⋅5 42⋅1
32⋅6 42⋅4 38⋅3 34⋅7 37⋅5 38⋅5 32⋅8 36⋅3 40⋅5
Reference Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) L’Abée-Lund et al. (1989)
north. Tamate & Maekawa (2006) found that SSD increased with increasing latitude in O. masou. They linked this to sex-biased anadromy, i.e. the proportion of non-anadromous precocious males decreased with increasing latitude. Male competition would be less intense at southerly latitudes where most males become non-anadromous precocious males, possibly because of improved growth opportunities in fresh relative to salt water (Gross et al., 1988). Thus, S. trutta exhibited populations with female-biased SSD , no SSD or male-biased SSD , the slope of the regression of female on male LT was 0⋅59 in agreement with Rensch’s (1960) rule. Sexual selection has been suggested as the reason for the allometry in male and female LT (Young, 2005). Probably, female choice influences male reproductive success in Salmo spp. (Järvi, 1990). For instance, females may prefer to mate with large males displaying the most extreme secondary sexual characteristics (Petersson et al., 1999). The observation that females were the largest sex in populations spawning in small streams and males were largest when occurring in larger rivers, however, cannot be explained by sexual selection alone. In mammals, female-biased SSD is most adequately explained by reduced male–male competition (Isaak, 2005). In S. trutta too, male–male competition may be reduced in small, but not in large streams. This hypothesis is supported by the fact that body size at maturity increases with stream flow in small, but not in large streams (L’Abée-Lund et al., 1989; Jonsson et al., 2001), indicating that stream size may be a constraint for fish size. A similar relationship between stream size and fish size was reported for Atlantic salmon Salmo salar L. 1758 (Schaffer & Elson, 1975; Jonsson et al., 1991). These species exhibit similar reproductive behaviours (Fleming, 1996; Jonsson & Jonsson, 2011). Possibly, the size of males more than females is constrained in small streams because males fight intensively in the spawning area, and narrow streams and low flow may limit the competitive success of large males more than of smaller males. Females show little aggression during spawning (Fleming et al., 1996), and the reproductive success of large females may not be constrained in small streams to the same degree as for large males. Thus, the strength of sexual selection on male body size may vary with the size of streams, and low flow may be a prime reason for why S. trutta males are smaller than females in small streams, but not in large streams. A similar relationship between SSD © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
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(a) 4·2
ln LTF (cm)
4·0
3·8
3·6
3·4 3·0 3·25 3·5 3·75 4·0 4·25 ln LTM (cm)
(b)
(c)
SSD
1·05
0·95
0·85
–4·0
–2·0
0 ln Q
2·0
4·0
6·0
60
(m3 s–1)
65
70
Latitude (° N)
Fig. 1. Regressions of (a) ln female total length (ln LTF ) on ln male total length (ln LTM ): y = 0⋅590x + 1⋅595 (r2 = 0⋅71, F 1,50 = 120⋅0, P < 0⋅001), (b) sexual size dimorphism (SSD ) on water flow (Q): y = 0⋅008x + 0⋅970 (r2 = 0⋅28, F 1,50 = 19⋅7, P < 0⋅001) and (c) SSD on latitude (∘ N): y = 0⋅004x + 0⋅700 (r2 = 0⋅16, F 1,50 = 9⋅2, P < 0⋅01) of 52 Norwegian populations of anadromous Salmo trutta. The locations and background variables are given in Table I.
and male size at maturity is expected to hold among populations of other stream spawning salmonids, such as S. salar. References Andersson, M. (1994). Sexual Selection. Princeton, NJ: Princeton University Press. Blankenhorn, W. U. (2005). Behavioural causes and consequences of sexual size dimorphism. Ethology 111, 977–1016. doi: 10.1111/j.1439-0310.2005.01147.x Caballero, P., Cobo, F. & González, M. A. (2006). Life history of sea trout (Salmo trutta) populations from the north-west Iberian Peninsula (River Ulla, Galicia, Spain). In Sea Trout: Biology, Conservation and Management (Harris, G. & Milner, N., eds), pp. 248–254. Oxford: Blackwell Publishing. Darwin, C. (1871). The Descent of Man, and Selection in Relation to Sex. London: John Murray.
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
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Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28, 659–687. doi: 10.1146/annurev.ecolsys.28.1.659 Finstad, A. G. & Hein, C. L. (2012). Migrate or stay: terrestrial primary productivity and climate drive anadromy in Arctic char. Global Change Biology 18, 2487–2497. doi: 10.1111/j.1365-2486.2012.02717.x Fleming, I. A. (1996). Reproductive strategies of Atlantic salmon: ecology and evolution. Reviews in Fish Biology and Fisheries 6, 379–416. doi: 10.1007/BF00164323 Fleming, I. A., Jonsson, B., Gross, M. R. & Lamberg, A. (1996). An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). Journal of Applied Ecology 33, 893–905. Gross, M. R., Coleman, R. M. & McDowall, R. M. (1988). Aquatic productivity and the evolution of diadromous fish migration. Science 239, 1291–1293. doi: 10.1126/science.239. 4845.1291 Hedrick, A. V. & Temeles, E. J. (1989). The evolution of sexual dimorphism in animals: Hypotheses and tests. Trends in Ecology and Evolution 4, 136–138. doi: 10.1016/01695347(89)90212-7 Hirst, A. G. & Kiørboe, T. (2014). Macroevolutionary patterns of sexual size dimorphism in copepods. Proceedings of the Royal Society B 281, 20140739. doi: 10.1098/rspb.2014. 0739 Isaak, J. L. (2005). Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal Review 35, 101–115. doi: 10.1111/j.1365-2907.2005.00045.x Järvi, T. (1990). The effects of male dominance, secondary sexual characteristics and female mate choice on the mating success of male Atlantic salmon Salmo salar. Ethology 84, 123–132. doi: 10.1111/j.1439-0310.1990.tb00789.x Jensen, K. W. (1968). Sea trout of the River Istra, Western Norway. Institute of Freshwater Research Drottningholm 48, 187–213. Jonsson, B. (1985). Life history patterns of freshwater resident and sea-run migrant brown trout in Norway. Transactions of the American Fisheries Society 114, 182–194. doi: 10.1577/1548-8659(1985)1142.0.CO;2 Jonsson, B. & Jonsson, N. (2005). Lipid energy reserves influence life-history decision of Atlantic salmon (Salmo salar) and brown trout (S. trutta) in fresh water. Ecology of Freshwater Fish 14, 296–301. doi: 10.1111/j.1600-0633.2005.00098.x Jonsson, B. & Jonsson, N. (2011). Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories. Dordrecht: Springer Science. Jonsson, N., Hansen, L. P. & Jonsson, B. (1991). Variation in age, size and repeat spawning of adult Atlantic salmon in relation to river discharge. Journal of Animal Ecology 60, 937–947. doi: 10.2307/5423 Jonsson, B., Jonsson, N., Brodtkorb, E. & Ingebrigtsen, P. J. (2001). Life history traits of brown trout vary with the size of small streams. Functional Ecology 15, 310–317. doi: 10.1046/j.1365-2435.2001.00528.x Kraushaar, U. & Blankenhorn, W. U. (2002). Population variation in sexual selection and its effects on size allometry in two dung fly species with contrasting sexual size dimorphism. Evolution 56, 307–321. L’Abée-Lund, J. H. (1991). Variation within and between rivers in adult size and sea age at maturity of anadromous brown trout, Salmo trutta. Canadian Journal of Fisheries and Aquatic Sciences 48, 1015–1021. doi: 10.1139/f91-119 L’Abée-Lund, J. H., Jonsson, B., Jensen, A. J., Sættem, L. M., Heggberget, T. G., Johnsen, B. O. & Næsje, T. F. (1989). Latitudinal variation in life history characteristics of sea-run migrant brown trout Salmo trutta. Journal of Animal Ecology 58, 525–542. Lengkeek, W., Didderen, K., Côté, I. M., van der Zee, E. M., Snoek, R. C. & Reynolds, J. D. (2008). Plasticity in sexual size dimorphism and Rensch’s rule in Mediterranean blennies (Blenniidae). Canadian Journal of Zoology 86, 1173–1178. doi: 10.1139/Z08-103 Lisle, S. P. & Rowe, L. (2013). Correlated evolution of allometry and sexual dimorphism across higher taxa. American Naturalist 182, 630–639. doi: 10.1086/673282
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Petersson, E., Järvi, T., Olsén, H., Mayer, I. I. & Hedenskog, M. (1999). Male-male competition and female choice in brown trout. Animal Behaviour 57, 777–783. doi: 10.1006/anbe.1998.1043 Rensch, B. (1960). Evolution above the Species Level. New York, NY: Columbia University Press. Schaffer, W. M. & Elson, P. E. (1975). The adaptive significance of variation in life history among local populations of Atlantic salmon in North America. Ecology 56, 577–590. doi: 10.2307/1935492 Sokal, R. R. & Rohlf, F. J. (1981). Biometry, 2nd edn. New York, NY: W.H. Freeman Publishers. Tamate, T. & Maekawa, K. (2006). Latitudinal variation in sexual dimorphism of sea-run masu salmon Oncorhynchus masou. Evolution 60, 196–201. doi: 10.1111/j.0014-3820.2006. tb01094.x Young, K. A. (2005). Life-history variation and allometry for sexual size dimorphism in Pacific salmon and trout. Proceedings of the Royal Society B 272, 167–172. doi: 10.1098/ rspb.2004.2931
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
BRIEF COMMUNICATION Sexual size dimorphism in anadromous brown trout Salmo trutta B. Jonsson* and N. Jonsson Norwegian Institute for Nature Research, Gaustadalléen 21, 0349 Oslo, Norway (Received 16 January 2014, Accepted 20 March 2015) Anadromous trout Salmo trutta exhibits sexual size dimorphism (SSD ); females were larger than males in populations where male mean total length (LT ) at maturity was below 49 cm and females were smaller than males when mean male LT was above 49 cm, the slope of the regression of female on male LT was 0⋅59. In streams with mean annual discharge below 41 m3 s−1 , flow added significantly to a model with SSD as the dependent variable and male mean LT at maturity as the first predictor variable. There was a slight increase in SSD with increasing latitude, which may result from an increase in male size with increasing latitude. © 2015 The Fisheries Society of the British Isles
Key words: allometry; latitudinal cline; length at maturity; water flow.
Sexual size dimorphism (SSD ) is common in animals (Hedrick & Temeles, 1989; Blankenhorn, 2005). Males are often larger than females in birds and mammals, whereas females are typically the larger sex in invertebrates and poikilothermic vertebrates such as fishes (Andersson, 1994; Hirst & Kiørboe, 2014). Large females may be favoured through natural selection because fecundity and reproductive success increase with increasing body size. Large males may be favoured both through natural and sexual selection (Darwin, 1871); through natural selection because milt production increases with body size (Jonsson & Jonsson, 2005) and large males may be superior competitors on the breeding grounds (Fleming et al., 1996); through sexual selection because large males may be favoured by females (Järvi, 1990; Jonsson & Jonsson, 2011). When not environmentally constrained, large males have access to more females and perform a higher number of spawnings than smaller conspecifics (Fleming et al., 1996). According to Rensch’s rule (Rensch, 1960), male body size varies more than female body size, and SSD typically increases with body size when males are largest, but decreases with increasing size when females are largest (Lengkeek et al., 2008; Lisle & Rowe, 2013). Thus, among conspecific populations, the slope usually is 1 for male-biased and 0⋅05) or ln Q (P > 0⋅05) as the first independent variable. The clinal increase of SSD with latitude appeared to be caused by an increase in male size towards the © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
S E X U A L D I M O R P H I S M I N S A L M O T R U T TA
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Table I. Streams with latitude, annual average flow, latitude and male and female mean total length (LT ) at maturity of Norwegian anadromous Salmo trutta, and reference to the study where the data were collected Location Tana Halselva Alta Skibotnelva Salangselva Hellemoelva Kobbelv Saltdalselva Beiarelva Ranaelva Vefsna Åbjøra Almåselva Mølleelva Norddalselva Skeitjørnbekken Vikabekken Børsethelva Råelva Hofstadelva Klefstadbekken Storelva Botna Herjåa Loddbekken Malma Bævra Eira Driva Istra Korsbrekkelva Ommedalselva Jostedøla Lærdalselva Aurlandselva Dyrvo Granvinselva Eio Ørbekken Imsa Langangselva Østeråbekken Allemanns-bekken
Latitude (∘ N) 70⋅22 70⋅02 69⋅58 69⋅23 68⋅52 67⋅48 67⋅37 67⋅07 67⋅02 66⋅20 65⋅50 65⋅04 64⋅28 64⋅28 64⋅28 64⋅28 64⋅28 63⋅32 63⋅32 63⋅30 63⋅26 63⋅26 63⋅20 63⋅20 63⋅20 63⋅20 63⋅02 62⋅40 62⋅39 62⋅33 62⋅07 61⋅44 61⋅23 61⋅07 60⋅54 60⋅37 60⋅32 60⋅22 58⋅59 58⋅53 58⋅30 58⋅30 58⋅23
Flow (m3 s−1 ) 167 5 73 15 23 7 26 55 40 83 137 19 0⋅49 0⋅18 1⋅24 0⋅15 0⋅27 0⋅11 0⋅11 0⋅21 0⋅17 0⋅24 0⋅16 0⋅92 0⋅16 0⋅27 14 15 68 4 9 70 70 39 39 1⋅00 3 44 0⋅35 5⋅1 0⋅30 0⋅10 0⋅05
Male LT (cm)
Female LT (cm)
46⋅5 41⋅7 42⋅5 42⋅8 47⋅1 52⋅0 35⋅0 61⋅9 44⋅8 48⋅6 41⋅9 44⋅5 41⋅3 33⋅5 37⋅7 43⋅9 35⋅5 36⋅3 35⋅3 38⋅2 35⋅2 36⋅9 36⋅6 52⋅7 36⋅7 47⋅6 30⋅6 44⋅2 52⋅3 52⋅1 45⋅8 46⋅4 59⋅7 54⋅7 75⋅8 42⋅0 41⋅2 41⋅3 36⋅7 35⋅7 33⋅7 24⋅7 25⋅4
39⋅9 47⋅1 44⋅1 50⋅1 51⋅8 49⋅0 45⋅1 56⋅6 45⋅1 46⋅8 46⋅0 42⋅9 41⋅9 36⋅2 42⋅3 42⋅8 38⋅8 36⋅1 40⋅2 40⋅8 39⋅7 37⋅0 42⋅7 53⋅3 43⋅0 53⋅2 45⋅9 43⋅2 45⋅4 50⋅7 47⋅4 51⋅4 52⋅3 52⋅3 63⋅7 44⋅9 44⋅5 41⋅0 42⋅4 43⋅8 38⋅8 30⋅7 34⋅0
© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
Reference L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund (1991) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) Jensen (1968) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) Jonsson (1985) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) L’Abée-Lund et al. (1989) Jonsson et al. (2001) Jonsson et al. (2001)
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Table I. Continued Location Grefstadbekken Mørfjærbekken Sævlibekken Helldalselva Slimestad-bekken Vesbekken Dårøybekken Røyseland-bekken Audna
Latitude (∘ N) 58⋅22 58⋅22 58⋅22 58⋅19 58⋅17 58⋅12 58⋅07 58⋅06 58⋅05
Flow (m3 s−1 ) 0⋅04 0⋅18 0⋅05 0⋅25 0⋅43 0⋅36 0⋅13 0⋅08 22
Male LT (cm)
Female LT (cm)
29⋅1 29⋅8 19⋅9 24⋅4 30⋅7 28⋅6 29⋅9 28⋅5 42⋅1
32⋅6 42⋅4 38⋅3 34⋅7 37⋅5 38⋅5 32⋅8 36⋅3 40⋅5
Reference Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) Jonsson et al. (2001) L’Abée-Lund et al. (1989)
north. Tamate & Maekawa (2006) found that SSD increased with increasing latitude in O. masou. They linked this to sex-biased anadromy, i.e. the proportion of non-anadromous precocious males decreased with increasing latitude. Male competition would be less intense at southerly latitudes where most males become non-anadromous precocious males, possibly because of improved growth opportunities in fresh relative to salt water (Gross et al., 1988). Thus, S. trutta exhibited populations with female-biased SSD , no SSD or male-biased SSD , the slope of the regression of female on male LT was 0⋅59 in agreement with Rensch’s (1960) rule. Sexual selection has been suggested as the reason for the allometry in male and female LT (Young, 2005). Probably, female choice influences male reproductive success in Salmo spp. (Järvi, 1990). For instance, females may prefer to mate with large males displaying the most extreme secondary sexual characteristics (Petersson et al., 1999). The observation that females were the largest sex in populations spawning in small streams and males were largest when occurring in larger rivers, however, cannot be explained by sexual selection alone. In mammals, female-biased SSD is most adequately explained by reduced male–male competition (Isaak, 2005). In S. trutta too, male–male competition may be reduced in small, but not in large streams. This hypothesis is supported by the fact that body size at maturity increases with stream flow in small, but not in large streams (L’Abée-Lund et al., 1989; Jonsson et al., 2001), indicating that stream size may be a constraint for fish size. A similar relationship between stream size and fish size was reported for Atlantic salmon Salmo salar L. 1758 (Schaffer & Elson, 1975; Jonsson et al., 1991). These species exhibit similar reproductive behaviours (Fleming, 1996; Jonsson & Jonsson, 2011). Possibly, the size of males more than females is constrained in small streams because males fight intensively in the spawning area, and narrow streams and low flow may limit the competitive success of large males more than of smaller males. Females show little aggression during spawning (Fleming et al., 1996), and the reproductive success of large females may not be constrained in small streams to the same degree as for large males. Thus, the strength of sexual selection on male body size may vary with the size of streams, and low flow may be a prime reason for why S. trutta males are smaller than females in small streams, but not in large streams. A similar relationship between SSD © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, doi:10.1111/jfb.12704
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(a) 4·2
ln LTF (cm)
4·0
3·8
3·6
3·4 3·0 3·25 3·5 3·75 4·0 4·25 ln LTM (cm)
(b)
(c)
SSD
1·05
0·95
0·85
–4·0
–2·0
0 ln Q
2·0
4·0
6·0
60
(m3 s–1)
65
70
Latitude (° N)
Fig. 1. Regressions of (a) ln female total length (ln LTF ) on ln male total length (ln LTM ): y = 0⋅590x + 1⋅595 (r2 = 0⋅71, F 1,50 = 120⋅0, P < 0⋅001), (b) sexual size dimorphism (SSD ) on water flow (Q): y = 0⋅008x + 0⋅970 (r2 = 0⋅28, F 1,50 = 19⋅7, P < 0⋅001) and (c) SSD on latitude (∘ N): y = 0⋅004x + 0⋅700 (r2 = 0⋅16, F 1,50 = 9⋅2, P < 0⋅01) of 52 Norwegian populations of anadromous Salmo trutta. The locations and background variables are given in Table I.
and male size at maturity is expected to hold among populations of other stream spawning salmonids, such as S. salar. References Andersson, M. (1994). Sexual Selection. Princeton, NJ: Princeton University Press. Blankenhorn, W. U. (2005). Behavioural causes and consequences of sexual size dimorphism. Ethology 111, 977–1016. doi: 10.1111/j.1439-0310.2005.01147.x Caballero, P., Cobo, F. & González, M. A. (2006). Life history of sea trout (Salmo trutta) populations from the north-west Iberian Peninsula (River Ulla, Galicia, Spain). In Sea Trout: Biology, Conservation and Management (Harris, G. & Milner, N., eds), pp. 248–254. Oxford: Blackwell Publishing. Darwin, C. (1871). The Descent of Man, and Selection in Relation to Sex. London: John Murray.
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Fairbairn, D. J. (1997). Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annual Review of Ecology and Systematics 28, 659–687. doi: 10.1146/annurev.ecolsys.28.1.659 Finstad, A. G. & Hein, C. L. (2012). Migrate or stay: terrestrial primary productivity and climate drive anadromy in Arctic char. Global Change Biology 18, 2487–2497. doi: 10.1111/j.1365-2486.2012.02717.x Fleming, I. A. (1996). Reproductive strategies of Atlantic salmon: ecology and evolution. Reviews in Fish Biology and Fisheries 6, 379–416. doi: 10.1007/BF00164323 Fleming, I. A., Jonsson, B., Gross, M. R. & Lamberg, A. (1996). An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). Journal of Applied Ecology 33, 893–905. Gross, M. R., Coleman, R. M. & McDowall, R. M. (1988). Aquatic productivity and the evolution of diadromous fish migration. Science 239, 1291–1293. doi: 10.1126/science.239. 4845.1291 Hedrick, A. V. & Temeles, E. J. (1989). The evolution of sexual dimorphism in animals: Hypotheses and tests. Trends in Ecology and Evolution 4, 136–138. doi: 10.1016/01695347(89)90212-7 Hirst, A. G. & Kiørboe, T. (2014). Macroevolutionary patterns of sexual size dimorphism in copepods. Proceedings of the Royal Society B 281, 20140739. doi: 10.1098/rspb.2014. 0739 Isaak, J. L. (2005). Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal Review 35, 101–115. doi: 10.1111/j.1365-2907.2005.00045.x Järvi, T. (1990). The effects of male dominance, secondary sexual characteristics and female mate choice on the mating success of male Atlantic salmon Salmo salar. Ethology 84, 123–132. doi: 10.1111/j.1439-0310.1990.tb00789.x Jensen, K. W. (1968). Sea trout of the River Istra, Western Norway. Institute of Freshwater Research Drottningholm 48, 187–213. Jonsson, B. (1985). Life history patterns of freshwater resident and sea-run migrant brown trout in Norway. Transactions of the American Fisheries Society 114, 182–194. doi: 10.1577/1548-8659(1985)1142.0.CO;2 Jonsson, B. & Jonsson, N. (2005). Lipid energy reserves influence life-history decision of Atlantic salmon (Salmo salar) and brown trout (S. trutta) in fresh water. Ecology of Freshwater Fish 14, 296–301. doi: 10.1111/j.1600-0633.2005.00098.x Jonsson, B. & Jonsson, N. (2011). Ecology of Atlantic Salmon and Brown Trout: Habitat as a Template for Life Histories. Dordrecht: Springer Science. Jonsson, N., Hansen, L. P. & Jonsson, B. (1991). Variation in age, size and repeat spawning of adult Atlantic salmon in relation to river discharge. Journal of Animal Ecology 60, 937–947. doi: 10.2307/5423 Jonsson, B., Jonsson, N., Brodtkorb, E. & Ingebrigtsen, P. J. (2001). Life history traits of brown trout vary with the size of small streams. Functional Ecology 15, 310–317. doi: 10.1046/j.1365-2435.2001.00528.x Kraushaar, U. & Blankenhorn, W. U. (2002). Population variation in sexual selection and its effects on size allometry in two dung fly species with contrasting sexual size dimorphism. Evolution 56, 307–321. L’Abée-Lund, J. H. (1991). Variation within and between rivers in adult size and sea age at maturity of anadromous brown trout, Salmo trutta. Canadian Journal of Fisheries and Aquatic Sciences 48, 1015–1021. doi: 10.1139/f91-119 L’Abée-Lund, J. H., Jonsson, B., Jensen, A. J., Sættem, L. M., Heggberget, T. G., Johnsen, B. O. & Næsje, T. F. (1989). Latitudinal variation in life history characteristics of sea-run migrant brown trout Salmo trutta. Journal of Animal Ecology 58, 525–542. Lengkeek, W., Didderen, K., Côté, I. M., van der Zee, E. M., Snoek, R. C. & Reynolds, J. D. (2008). Plasticity in sexual size dimorphism and Rensch’s rule in Mediterranean blennies (Blenniidae). Canadian Journal of Zoology 86, 1173–1178. doi: 10.1139/Z08-103 Lisle, S. P. & Rowe, L. (2013). Correlated evolution of allometry and sexual dimorphism across higher taxa. American Naturalist 182, 630–639. doi: 10.1086/673282
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