Bergmann's idiosyncratic rule: a role for fecundity selection?

Authors


Gavin H. Thomas, Fax: +44 (0)1344 873173; E-mail: g.thomas@imperial.ac.uk

Abstract

The negative relationship between temperature and geographical variation in body size, or Bergmann's rule, is among the most thoroughly studied ecogeographical rules, yet the pattern and process underlying it remain controversial. Bergmann's original observations were of body size clines among endotherms, but in the last 50 years there has been increasing recognition that both Bergmann's rule and its reverse occur in many ectotherm taxa. A new study of syngnathid fish by Wilson (2009) in this issue of Molecular Ecology sheds light on intriguing alternative mechanisms that may explain variation in the direction of body size clines across taxa. Wilson shows that Bergmann's rule is found in pipefish of the genus Syngnathus, but not in seahorses of the genus Hippocampus. His results suggest that polygamy in pipefish allows fecundity selection to favour large size at low temperatures, compensating for increases in brooding time.

The mechanisms that underlie Bergmann's rule, a negative relationship between temperature and body size (Bergmann 1847), have been controversial for decades (reviewed in Blackburn et al. 1999; Meiri & Thomas 2007). Bergmann observed that smaller-bodied endotherms in general inhabit warmer areas than larger-bodied species and proposed that this was because the smaller surface area to volume ratios of larger bodied species would be favoured at low temperatures (Bergmann 1847). However, while Bergmann referred exclusively to warm-blooded vertebrates, the rule is neither ubiquitous among, nor restricted to, endotherms (Ray 1960; Lindsey 1966; Blackburn et al. 1999; Ashton & Feldman 2003) implying that the heat conservation mechanism is not general (Blackburn et al. 1999; Pincheira-Donoso et al. 2008). In particular, it is not obvious why the heat conservation hypothesis should apply to cold-blooded organisms (Pincheira-Donoso et al. 2008), and there is evidence for both Bergmann's rule and its reverse in ectotherms (Blanckenhorn et al. 2006). Explaining geographical variation in body size with respect to temperature across taxa evidently requires multiple mechanisms. In a study of syngnathid fishes (seahorses and pipefish) published in this issue of Molecular Ecology, Wilson (2009) reveals unexpected links between sexual and fecundity selection and the evolution of body size clines.

Fecundity is known to increase with body size in seahorses (Foster & Vincent 2004) and Wilson shows how variation in fecundity selection can generate body size gradients that are consistent with Bergmann's rule. In both seahorses and pipefish, the males brood the developing embryos, but while seahorses are monogamous and brood the eggs of only one female at a time, pipefish are polygamous and brood eggs of multiple females (Fig. 1A). This fundamental difference in breeding behaviour may explain why Wilson finds that body size increases with latitude (as a proxy for temperature) in pipefish (Fig. 1B) but not in seahorses. Male seahorse reproductive rate is limited by the fecundity of his mate, whereas the number of matings limits male pipefish reproductive rate. If male size limits the number of embryos that can be brooded, then fecundity selection should favour large male size in pipefish but not in seahorses. This leaves open the question of why male pipefish are not larger at low latitudes where presumably larger size would also increase the number of embryos that can be brooded. Wilson suggests that body size might in general remain small at lower latitudes in iteroparous species due to the long-term fecundity advantages of early maturation. However, in pipefish, brooding time varies along temperature gradients: in one species of pipefish Syngnathus typhle, a reduction in water temperature of only 5 °C increases brooding time from 35 to 58 days (Ahnesjö 1995). Thus, at low temperatures fecundity selection may favour larger male size because it may help to maintain the potential reproductive rate (PRR; the number of offspring produced per day). Wilson tests this hypothesis by examining variation in body size, fecundity, and number of matings along a latitudinal gradient in the pipefish Syngnathus leptorhynchus. He finds first that Bergmann's rule is present at the intraspecific level, and second, that the PRR of males is similar in each population along a latitudinal gradient.

Figure 1 (A).

Picture of a pregnant male pipefish Syngnathus typhle (photo courtesy of Valeria Rispoli), and (B) latitudinal size variation in male and female S. leptorhynchus (AK: Sitka Alaska; WA: Padilla Bay, Washington; OR: Newport, Oregon; CA: San Diego, California; photo courtesy of Tony Wilson).

How general might these results be? Pipefish are clearly unusual in that the males are polygamous and brood the young (Berglund & Rosenqvist 2003), and polygamy may be a key requirement for fecundity to generate body size gradients. If we assume (or preferably demonstrate empirically) that developmental time of the offspring, or juvenile mortality, increases with declining temperature such that the PRR drops, then large body size should be favoured if it enables more offspring to be produced or brooded. The most direct route to maintaining PRR would be for females to increase egg production, as may be the case in S. typhle, although Wilson found no significant relationship between female body size and fecundity in S. leptorhynchus. However, since the PRR can also be maintained by multiple mating, large body size should be favoured in the sex that cares for (i.e. broods or incubates) the offspring. It is reasonable to ask why, among syngnathid fish, polygamy has not evolved in the seahorse clade since presumably this would be advantageous. Previous research has argued that multiple mating in seahorses may be limited by both the behavioural constraints imposed by mating synchronization (Vincent et al. 2004) and by physiological limits to multiple mating (Wilson & Martin-Smith 2007). Behavioural traits are often considered to be evolutionarily labile (Blomberg et al. 2003) and mating behaviour varies within species of some taxa (e.g. shorebirds, Thomas et al. 2007), suggesting that the clade-wide pattern of monogamy is more likely to be due to phylogenetically conserved physiological limits than to behavioural constraints. Alternatively, declines in temperature may not increase brooding time in seahorses to the extent that it appears to in pipefish, and selection to maintain PRR may be weak. It would be interesting to explore the intraspecific pattern of body size for seahorses since experimental evidence from the yellow seahorse Hippocampus kuda suggests that male size influences offspring survival and future fitness (Dzyuba et al. 2006).

Intriguingly, if maintenance of the PRR drives selection for larger body size, then the slope of the body size gradient is expected to differ between the sexes: where only one sex broods or incubates the offspring, the body size–temperature gradient should be steepest (more negative) in the care-giving sex. In pipefish, the pattern of Bergmann's rule should therefore be most pronounced in males. An obvious emergent outcome would be a cline in sexual size dimorphism (SSD) with increasing dimorphism towards the caring sex at lower temperatures. An equivalent of Bergmann's rule for SSD was recently shown to have only weak support within species (Blanckenhorn et al. 2006). However, the authors noted that temperature gradients in SSD may be more prevalent between rather than within species where differences in sexual selection may be more important. Rispoli & Wilson (2008) found no evidence for male or female size increases with latitude in the polygamous pipefish S. typhle but noted the frequent occurrence of female-biased SSD. The presence of any interspecific latitudinal gradient in SSD will clearly be influenced by many factors. For example, the relative importance of sexual selection and natural selection acting on body size (e.g. Székely et al. 2004), and the strength of any genetic correlation between male and female body size (Lande 1980) will likely influence the evolution of SSD.

Since the first tests of Bergmann's rule in ectotherms (Ray 1960; Lindsey 1966) and more extensive studies in endotherms, it has becoming increasingly clear that observations of patterns consistent with Bergmann's hypothesis are too idiosyncratic to be a general rule for animals. Indeed, as noted above, Bergmann's original conjecture was explicit in its focus on endotherms and an apparent repeated lack of support for Bergmann's rule in ectotherms has led to a reiteration of the idea that the rule should apply exclusively to endotherms (Pincheira-Donoso et al. 2008). Yet, Bergmann's rule is not even ubiquitous in endotherms and continued focus on finding and explaining the ‘rule’ may hamper our understanding of the processes that generate geographical gradients in body size. Studies such as Wilson's in this issue offer important new insights by using combined intra- and interspecific approaches, to test the roles of natural, sexual, and fecundity selection in producing environmental gradients in key life-history traits.

Acknowledgements

I thank Tony Wilson, Nolan Kane and Shai Meiri for comments on this manuscript, and Valeria Rispoli and Tony Wilson for kindly preparing and providing photos.

Gavin Thomas is an evolutionary biologist. His current research focuses on the processes that determine large-scale macroevolutionary and macroecological trends in species traits. He also has interests in sexual conflict over parental care and the evolution of breeding systems, particularly in shorebirds.

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