Testing mechanisms of Bergmann's rule: phenotypic decline but no genetic change in body size in three passerine bird populations

Bergmann's rule predicts a decrease in body size with increasing temperature and has much empirical support. Surprisingly, we know very little about whether "Bergmann size clines" are due to a genetic response or are a consequence of phenotypic plasticity. Here, we use data on body size (mass and tarsus length) from three long-term (1979-2008) study populations of great tits (Parus major) that experienced a temperature increase to examine mechanisms behind Bergmann's rule. We show that adult body mass decreased over the study period in all populations and that tarsus length increased in one population. Both body mass and tarsus length were heritable and under weak positive directional selection, predicting an increase, rather than a decrease, in body mass. There was no support for microevolutionary change, and thus the observed declines in body mass were likely a result of phenotypic plasticity. Interestingly, this plasticity was not in direct response to temperature changes but seemed to be due to changes in prey dynamics. Our results caution against interpreting recent phenotypic body size declines as adaptive evolutionary responses to temperature changes and highlight the importance of considering alternative environmental factors when testing size clines.     

Inter-specific association and habitat use in a farmland passerine assemblage

We studied the pattern of inter-specific association of breeding territories in a passerine assemblage of dry cereal farmland in central Spain and evaluated the role of the presence of heterospecifics in the habitat use patterns exhibited by different species. Bird territories showed a non-random inter-specific spatial aggregation pattern. We studied territory abundance variation in the three more abundant species: the corn bunting, the crested lark, and the fan-tailed warbler. Crested lark and fan-tailed warbler territories were more abundant in plots where corn bunting territories were present and vice versa, while their respective abundances did not vary with the breeding presence of the other species. We used landscape and agricultural management variables to analyze the relationships between habitat and each species?? breeding territories by means of classification trees. While the corn bunting showed a marked pattern of nesting habitat use, the crested lark and the fan-tailed warbler exhibited a much more generalist one. Corn Bunting presence was affected negatively by intensification-related variables, such as field size and percent cover of cereal crops. Similarly, the presence of crested larks was negatively related to high yielding areas. However, when the presence of hetero-specific territories was considered, the presence of corn bunting territories was the most important variable explaining the occurrence of breeding fan-tailed warblers, and the second most important in the case of the crested lark. These results suggest that inter-specific attraction could play a role in the formation of farmland bird assemblages, while adding further evidence for the detrimental effect of agricultural intensification at the community level.     

Recent changes in body weight and wing length among some British passerine birds

We tested the prediction that global warming has caused recent decreases in body weight (Bergmann's rule) and increases in wing length (Allen's rule) in 14 species of passerine birds at two localities in England: Wicken Fen (1968–2003) and Treswell Wood (1973–2003).
Predicted long-term linear decreases in residual body weight occurred in four species: dunnocks (Wicken Fen), and great tits, blue tits and bullfinches (Treswell Wood). Non-linear decreases also occurred in reed warblers and blackcaps at Wicken Fen, which also had a surprising linear increase in residual body weight in blackbirds.
Residual wing lengths increased linearly, as predicted, in six of seven species at Wicken Fen. Whereas there were non-linear long-term increases in wrens, dunnocks and blackbirds in Treswell Wood. Unexpected linear decreases also occurred in residual wing lengths in willow warblers (Wicken Fen), and blue tits, great tits and chaffinches (Treswell Wood).
The most parsimonious explanation for such long-term changes in body weight is global warming, as predicted by Bergmann's rule. Greater site and species-specific effects on wing length (e.g. non-linear changes plus shorter wings in the woodland habitat) suggest a less straightforward conclusion concerning Allen's rule, probably because wing length involved variation in both bone and feather growth.
Changes in residual body weights and wing lengths often differed between species and were sometimes non-linear, perhaps reflecting short-term modifications in selection pressures. Human-induced influences are discussed, such as avian predator population densities and land-use change. Short-term variation in temperature had little effect, but rainfall did explain the unusual increase in blackbird body weight, possibly as a result of improving food (earthworm) availability.     

Bergmann's rule in nonavian reptiles: turtles follow it,lizards and snakes reverse it

Abstract Bergmann's rule is currently defined as a within-species tendency for increasing body size with increasing latitude or decreasing environmental temperature. This well-known ecogeographic pattern has been considered a general trend for all animals, yet support for Bergmann's rule has only been demonstrated for mammals and birds. Here we evaluate Bergmann's rule in two groups of reptiles: chelonians (turtles) and squamates (lizards and snakes). We perform both nonphylogenetic and phylogenetic analyses and show that chelonians follow Bergmann's rule (19 of 23 species increase in size with latitude; 14 of 15 species decrease in size with temperature), whereas squamates follow the converse to Bergmann's rule (61 of 83 species decrease in size with latitude; 40 of 56 species increase in size with temperature). Size patterns of chelonians are significant using both nonphylogenetic and phylogenetic methods, whereas only the nonphylogenetic analyses are significant for squamates. These trends are consistent among major groups of chelonians and squamates for which data are available. This is the first study to document the converse to Bergmann's rule in any major animal group as well as the first to show Bergmann's rule in a major group of ectotherms. The traditional explanation for Bergmann's rule is that larger endothermic individuals conserve heat better in cooler areas. However, our finding that at least one ectothermic group also follows Bergmann's rule suggests that additional factors may be important. Several alternative processes, such as selection for rapid heat gain in cooler areas, may be responsible for the converse to Bergmann's rule in squamates.     

The effect of island area on body size in a primate species from the Sunda Shelf Islands

Aim  We examine the effect of island area on body dimensions in a single species of primate endemic to Southeast Asia, the long-tailed macaque ( Macaca fascicularis ). In addition, we test Allen's rule and a within-species or intraspecific equivalent of Bergmann's rule (i.e. Rensch's rule) to evaluate body size and shape evolution in this sample of insular macaques.
Location  The Sunda Shelf islands of Southeast Asia.
Methods  Body size measurements of insular macaques gathered from the literature were analysed relative to island area, latitude, maximum altitude, isolation from the mainland and other islands, and various climatic variables using linear regression.
Results  We found no statistically significant relationship between island area and body length or head length in our sample of insular long-tailed macaques. Tail length correlated negatively with island area. Head length and body length exhibited increases corresponding to increasing latitude, a finding seemingly consistent with the expression of Bergmann's rule within a single species. These variables, however, were not correlated with temperature, indicating that Bergmann's rule is not in effect. Tail length was not correlated with either temperature or increasing latitude, contrary to that predicted by Allen's rule.
Main conclusions  The island rule dictating that body size will covary with island area does not apply to this particular species of primate. Our study is consistent with results presented in the literature by demonstrating that skull and body length in insular long-tailed macaques do not, strictly speaking, conform to Rensch's rule. Unlike previous studies, however, our findings suggest that tail-length variation in insular macaques does not support Allen's rule.     

In silico peptide-binding predictions of passerine MHC class I reveal similarities across distantly related species, suggesting convergence on the level of protein function

The major histocompatibility complex (MHC) genes are the most polymorphic genes found in the vertebrate genome, and they encode proteins that play an essential role in the adaptive immune response. Many songbirds (passerines) have been shown to have a large number of transcribed MHC class I genes compared to most mammals. To elucidate the reason for this large number of genes, we compared 14 MHC class I alleles (α1–α3 domains), from great reed warbler, house sparrow and tree sparrow, via phylogenetic analysis, homology modelling and in silico peptide-binding predictions to investigate their functional and genetic relationships. We found more pronounced clustering of the MHC class I allomorphs (allele specific proteins) in regards to their function (peptide-binding specificities) compared to their genetic relationships (amino acid sequences), indicating that the high number of alleles is of functional significance. The MHC class I allomorphs from house sparrow and tree sparrow, species that diverged 10 million years ago (MYA), had overlapping peptide-binding specificities, and these similarities across species were also confirmed in phylogenetic analyses based on amino acid sequences. Notably, there were also overlapping peptide-binding specificities in the allomorphs from house sparrow and great reed warbler, although these species diverged 30 MYA. This overlap was not found in a tree based on amino acid sequences. Our interpretation is that convergent evolution on the level of the protein function, possibly driven by selection from shared pathogens, has resulted in allomorphs with similar peptide-binding repertoires, although trans-species evolution in combination with gene conversion cannot be ruled out.     

Bergmann's rule and the mammal fauna of northern North America

The observation that "on the whole…  larger species live farther north and the smaller ones farther south" was first published by Carl Bergmann in 1847. However, why animal body mass might show such spatial variation, and indeed whether it is a general feature of animal assemblages, is currently unclear. We discuss reasons for this uncertainty, and use our conclusions to direct an analysis of Bergmann's rule in the mammals in northern North America, in the communities of species occupying areas that were covered by ice at the last glacial maximum. First, we test for the existence of Bergmann's rule in this assemblage, and investigate whether small- and large-bodied species show different spatial patterns of body size variation. We then attempt to explain the spatial variation in terms of environmental variation, and evaluate the adequacy of our analyses to account for the spatial pattern using the residuals arising from our environmental models. Finally, we use the results of these models to test predictions of different hypotheses proposed to account for Bergmann's rule. Bergmann's rule is strongly supported. Both small- and large-bodied species exhibit the rule. Our environmental models account for most of the spatial variation in mean, minimum and maximum body mass in this assemblage. Our results falsify predictions of hypotheses relating to migration ability and random colonisation and diversification, but support predictions of hypotheses relating to both heat conservation and starvation resistance.     

Bergmann's rule; a concept cluster?

The science behind ecology has been contested for years, partially because of the misuse and misrepresentation of concepts within ecology. This paper discusses the use of Bergmann's rule, a fundamental rule of biogeography. The rule was proposed by Carl Bergmann in 1847 and was published only in German; therefore, the majority of researchers have relied on a single translation by Mayr suggesting that races from cooler climates tend to be larger in species of warm-blooded vertebrates than races of the same species living in warmer climates. That many scientists cannot go back to the original source of information because it has not been published in English has resulted in relying on others for interpretation and led to several problems, the largest of which is whether the definition of the rule should include the mechanism, which had been proposed by Bergmann. There has been a large field of research on the subject, but few tests of the mechanisms behind the observed phenomenon. We conducted a review of the literature on Bergmann's rule, and from this suggest (1) Bergmann's original rule be maintained (a direct translation is provided), (2) mechanism is inherent in Bergmann's rule and is required for a rule to be of scientific value; patterns should be labelled as trends, not rules, (3) the focus should be on falsifying hypothesized mechanisms rather than simply describing patterns, and (4) to truly evaluate Bergmann's rule in a scientific manner the original German source should be translated and made available to the scientific public.     

Fecundity selection predicts Bergmann's rule in syngnathid fishes

The study of latitudinal increases in organismal body size (Bergmann's rule) predates even Darwin's evolutionary theory. While research has long concentrated on identifying general evolutionary explanations for this phenomenon, recent work suggests that different factors operating on local evolutionary timescales may be the cause of this widespread trend. Bergmann's rule explains body size variation in a diversity of warm-blooded organisms and there is increasing evidence that Bergmann's rule is also widespread in ectotherms. Bergmann's rule acts differentially in species of the Syngnathidae, a family of teleost fishes noted for extreme adaptations for male parental care. While variation in body size of polygamous Syngnathus pipefish is consistent with Bergmann's rule, body size is uncorrelated with latitude in monogamous Hippocampus seahorses. A study of populations of Syngnathus leptorhynchus along a natural latitudinal and thermal gradient indicates that increases in body size with latitude maintain the potential reproductive rate of males despite significant decreases in ambient temperatures. Polygyny is necessary in order to maximize male reproductive success in S. leptorhynchus , suggesting a possible a link between fecundity selection and Bergmann's rule in this species.     

Carnivores, biases and Bergmann's rule

Studies of Bergmann's rule may encompass a non-random subsample of extant homeotherms. We examined patterns of correlation between skull length and geographical latitude in 44 species of carnivores in order to test the validity of Bergmann's rule in the Carnivora. Results were then compared to those of other studies. Significant positive correlation between skull length and latitude was found in 50% of carnivore species, while significant negative correlation was found in only 11% of species. These results indicate that the occurrence of Bergmann's rule in the Carnivora is less frequent than earlier published data suggest. Publication bias is not detected in published data. Therefore, previous studies of geographical size variation might be biased in favour of species known to follow Bergmann's rule.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 579–588.     

Amphibians do not follow Bergmann's rule

The tendency for organisms to be larger in cooler climates (Bergmann's rule) is widely observed in endotherms, and has been reputed to apply to some ectotherms including amphibians. However, recent reports provide conflicting support for the pattern, questioning whether Bergmann's clines are generally present in amphibians. In this study, we measured 96,996 adult Plethodon from 3974 populations to test for the presence of Bergmann's clines in these salamanders. Only three Plethodon species exhibited a significant negative correlation between body size and temperature consistent with Bergmann's rule, whereas 37 of 40 species did not display a pattern consistent with this prediction. Further, a phylogenetic comparative analysis found no relationship between body size and temperature among species. A meta-analysis combining our data with the available data for other amphibian species revealed no support for Bergmann's rule at the genus (Plethodon), order (Caudata), or class (Amphibia) levels. Our findings strongly suggest that negative thermal body size clines are not common in amphibians, and we conclude that Bergmann's rule is not generally applicable to these taxa. Thus, evolutionary explanations of Bergmann's clines in other tetrapods need not account for unique life-history attributes of amphibians.     

Body size evolution in South American Liolaemus lizards of the boulengeri clade: a contrasting reassessment

Bergmann's rule predicts larger body sizes in species living in higher latitudes and altitudes. This rule appears to be valid for endotherms, but its relevance to ectotherm vertebrates has largely been debated. In squamate reptiles (lizards and snakes), only one study, based on Liolaemus species of the boulengeri clade, has provided phylogenetic evidence in favour of Bergmann's clines. We reassessed this model in the same lizard clade, using a more representative measure of species body size and including a larger number of taxa in the sample. We found no evidence to support Bergmann's rule in this lineage. However, these non-significant results appear to be explained only by the inclusion of further species rather than by a different estimation of body size. Analyses conducted on the 16 species included in the previous study always revealed significant relationships between body size and latitude-altitude, whereas, the enlarged sample always rejected the pattern predicted by Bergmann's rule.     

The phylogeny of a species-level tendency: species heritability and possible deep origins of Bergmann's rule in tetrapods

One of the most widely recognized generalizations in biology is Bergmann's rule, the observation that, within species of birds and mammals, body size tends to be inversely related to ambient temperature. Recent studies indicate that turtles and salamanders also tend to follow Bergmann's rule, which hints that this species-level tendency originated early in tetrapod history. Furthermore, exceptions to Bergmann's rule are concentrated within squamate reptiles (lizards and snakes), suggesting that the tendency to express a Bergmann's rule cline may be heritable at the species level. We evaluated species-level heritability and early origination of Bergmann's rule by mapping size-latitude relationships for 352 species onto a tetrapod phylogeny. When the largest available dataset is used, Bergmann's rule shows significant phylogenetic signal, indicating species-level heritability. This represents one of the few demonstrations of heritability for an emergent species-level property and the first for an ecogeographic rule. When species are discretely coded as showing either Bergmann's rule or its converse, parsimony reconstructions suggest that: (1) the tendency to follow Bergmann's rule is ancestral for tetrapods, and (2) most extant species that express the rule have retained this tendency from that ancient ancestor. The first inference also generally holds when the discrete data or size-latitude correlation coefficients are analyzed using maximum likelihood, although the results are only statistically significant for some versions of the discrete analyses. The best estimates of ancestral states suggest that the traditional adaptive explanation for Bergmann's rule-conservation of metabolic heat-was not involved in the origin of the trait since that origin predates the evolution of endothermy. A more general thermoregulatory hypothesis could apply to endotherms and some ectotherms, but fails to explain why salamanders have retained Bergmann's rule. Thus, if thermoregulation underlies the origin of a Bergmann's rule tendency, this trait may have been continuously maintained while its cause changed. Alternatively, thermoregulation may not underlie Bergmann's rule in any tetrapod group. The results also suggest that many extinct groups not included in our analyses followed Bergmann's rule.     

Testing Bergmann's rule in the presence of potentially confounding factors: a case study with three species of Galerida larks in Morocco

Aim  To test Bergmann's rule (which predicts a larger body size in colder areas within warm-blooded vertebrate species) in three partially sympatric species of larks ( Galerida theklae , Galerida cristata and Galerida randonii ) that occur in Morocco.
Location  Morocco.
Methods  Restriction fragment length polymorphism techniques applied on cytochrome b haplotypes were used to discriminate G. cristata and G. randonii , and to investigate the effects of interspecific hybridization in their contact zone. A comprehensive statistical framework was then designed to test Bergmann's rule in our three Galerida species (using altitude as a proxy for cold temperatures), while controlling for the possible influence of interspecific hybridization and competition and accounting for spatial autocorrelation. The method we propose is conservative in the sense that potentially confounding factors are adjusted so as to maximize their influence on the variable of interest.
Results  Bergmann's rule was strongly supported in G. theklae and G. randonii . However, body size did not respond to altitude in G. cristata , a result that was not simply explained by species-specific differences in geographical ranges and altitudinal span. In G. cristata , we detected a tendency for body size to increase with aridity, in agreement with an alternative definition of Bergmann's rule. However, since G. cristata also hybridizes with G. randonii in a contact zone located in the most arid part of the range of G. cristata , we could not tease apart the relative contribution of selection and hybridization in driving this pattern.
Main conclusions  This study highlights the need for careful statistical designs that allow meaningful variables to be picked out from large sets of potential factors. When taking these factors into account, we found that Bergmann's rule was still strongly supported in two out of the three species examined.     

Variation and Sexual Dimorphism of Body Size in the Plateau Brown Frog along an Altitudinal Gradient

Variation in body size and sexual size dimorphism(SSD) can have important consequences for animal ecology, behavior, population dynamics and the evolution of life-history traits. Organisms are expected to be larger in colder climate(i.e., Bergmann's rule) and SSD varies with body size(i.e., Rensch's rule). However, the underlying mechanisms are still elusive. The plateau brown frog(Rana kukunoris), a medium-sized anuran species with femalebiased SSD, is endemic to the Qinghai-Tibetan Plateau(QTP). From 1797 m(Maoxiang'ping) to 3453 m(Heihe'qiao) in the eastern margin of the QTP, we surveyed 10 populations of R. kukunoris and collected phalanges and snout vent length(SVL) data for 258 adult individuals(199 males versus 59 females). Based on these data, we explored how body size and SSD varying along the altitudinal gradient and examined the corresponding effects of temperature. We found body size to be larger at higher altitude for males but not for females, with likely effects from the temperature on the variation in male body size. Sex differences in growth rates may be the main cause of the variation in SSD. Our results suggested that only males follow the Bergmann's rule and variation in SSD of R. kukunoris do not support the Rensch's rule and its inverse. Therefore, the variations of body size can be different between sexes and the applicability of both Bergmann's rule and Rensch's rule should depend on species and environment where they live.     

The importance of phylogenetic scale in tests of Bergmann's and Rapoport's rules: lessons from a clade of South American lizards

We tested for the occurrence of Bergmann's rule, the pattern of increasing body size with latitude, and Rapoport's rule, the positive relationship between geographical range size and latitude, in 34 lineages of Liolaemus lizards that occupy arid regions of the Andean foothills. We tested the climatic-variability hypothesis (CVH) by examining the relationship between thermal tolerance breadth and distribution. Each of these analyses was performed varying the level of phylogenetic inclusiveness. Bergmann's rule and the CVH were supported, but Rapoport's rule was not. More variance in the data for Bergmann's rule and the CVH was explained using species belonging to the L. boulengeri series rather than all species, and inclusion of multiple outgroups tended to obscure these macroecological patterns. Evidence for Bergmann's rule and the predicted patterns from the CVH remained after application of phylogenetic comparative methods, indicating a greater role of ecological processes rather than phylogeny in shaping the current species distributions of these lizards.     

Sexual size dimorphism and assortative mating for morphological traits in Passer domesticus

In this study, assortative mating for different morphological traits was studied in a captive population of house sparrows (Passer domesticus). Males were larger than females. Assortative mating was found for tail length, wing length and general body size. Males with larger badge size mated with females with longer tails. The strongest assortative mating occurred for tail length (r=0.77), and this assortative mating remained significant after controlling for wing length, mass and tarsus length, suggesting that it was not an artefact of assortative mating for body size. The possibility of sexual selection for tail length in the house sparrow is discussed.     

WHEN RENSCH MEETS BERGMANN: DOES SEXUAL SIZE DIMORPHISM CHANGE SYSTEMATICALLY WITH LATITUDE?

Bergmann's and Rensch's rules describe common large-scale patterns of body size variation, but their underlying causes remain elusive. Bergmann's rule states that organisms are larger at higher latitudes (or in colder climates). Rensch's rule states that male body size varies (or evolutionarily diverges) more than female body size among species, resulting in slopes greater than one when male size is regressed on female size. We use published studies of sex-specific latitudinal body size clines in vertebrates and invertebrates to investigate patterns equivalent to Rensch's rule among populations within species and to evaluate their possible relation to Bergmann's rule. Consistent with previous studies, we found a continuum of Bergmann (larger at higher latitudes: 58 species) and converse Bergmann body size clines (larger at lower latitudes: 40 species). Ignoring latitude, male size was more variable than female size in only 55 of 98 species, suggesting that intraspecific variation in sexual size dimorphism does not generally conform to Rensch's rule. In contrast, in a significant majority of species (66 of 98) male latitudinal body size clines were steeper than those of females. This pattern is consistent with a latitudinal version of Rensch's rule, and suggests that some factor that varies systematically with latitude is responsible for producing Rensch's rule among populations within species. Identifying the underlying mechanisms will require studies quantifying latitudinal variation in sex-specific natural and sexual selection on body size.     

Competition between birds and mammals: A comparison of giving-up densities between crested larks and gerbils

We combined the concept of mechanisms of co-existence with the approach of giving-up densities to study inter-taxon competition between seed-eating birds and mammals. We measured feeding behaviour in food patches to define and study the guild of seed-eating vertebrates occupying sandy habitats at Bir Asluj, Negev Desert, Israel. Despite a large number of putatively granivorous rodents and birds at the site, two gerbil species (Allenbys gerbil, Gerbillus allenbyi, and the greater Egyptian gerbil, G. pyramidum) dominated nocturnal foraging, and a single bird species (crested lark, Galerida cristata) contributed all of the daytime foraging. We used giving-up densities to quantify foraging behaviour and foraging efficiencies. A low giving-up density demonstrates the ability of a forager to profitably harvest food at low abundances and to profitably utilize the foraging opportunities left behind by the less efficient forager. Gerbils had lower giving-up densities in the bush than open microhabitat, and lower giving-up densities in the semi-stabilized than stabilized sand habitats. Crested larks showed the opposite: lower giving-up densities in the open than bush, and on the stabilized than semi-stabilized sand habitats. Despite these patterns, gerbils had substantially lower giving-up densities than crested larks in both microhabitats, all sand habitats, and during each month. Several mechanisms may permit the crested lark to co-exist with the gerbils. Larks may be cream skimmers on the high spatial and temporal variability in seed abundances. Larks may rely on insects, fruit or smaller seeds. Or, larks may rely on adjacent rocky habitats.     

Ecogeographic variation in body size and shape of Cape sparrows (Passer melanurus) in southern Africa

Canonical discriminant analyses were used to assess whether four populations of Cape sparrows varied in body size and shape according to predictions from Bergmann's Rule. In accordance with Bergmann's Rule, birds from two hot, arid Namib desert sites (Namib 1 and Namib 2) were smaller than birds from two cool, mesic Transvaal sites. If heat dissipation through extremities (tarsi) is important to reduce water lost from evaporative cooling, birds under hot conditions in dry environments (Namib 2) should have longer tarsi than those in more humid hot environments (Namib 1). Contrary to this, males at Namib 2 had relatively longer wings hut shorter tarsi than at Namib 1, and female relative tarsus length did not vary between desert sites