The island rule and the evolution of body size in the deep sea

Aim  Our goal is to test the generality of the island rule – a graded trend from gigantism in small-bodied species to dwarfism in large-bodied species – in the deep sea, a non-insular but potentially analogous system.
Location  Shallow-water and deep-sea benthic habitats in the western Atlantic Ocean from the North to South Poles.
Methods  We conducted regression analyses of body size of deep-sea gastropods species relative to their shallow-water congeners using measurements from the Malacolog ver. 3.3.3 database.
Results  Our results indicate that, consistent with the island rule, gastropod genera with small-bodied, shallow-water species have significantly larger deep-sea representatives, while the opposite is true for genera that are large-bodied in shallow water. Bathymetric body size clines within the deep sea are also consistent with predictions based on the island rule.
Main conclusions  Like islands, the deep sea is characterized by low absolute food availability, leading us to hypothesize that the island rule is a result of selection on body size in a resource-constrained environment. The body size of deep-sea species tends to converge on an optimal size for their particular ecological strategy and habitat.     

Optical parameters of euphausiid eyes as a function of habitat depth

Summary The relationships between habitat depth, eye diameter relative to body length, and the dimensions of rhabdoms and crystalline cones have been examined for 13 species of three oceanic euphausiid genera with habitats ranging from near-surface waters to the deep-sea. Rate of eye growth decreases with depth. Longer rhabdoms may increase the visual sensitivity to point and extended light sources by an eye of a particular size with depth. Larger interommatidial angles suggest that visual acuity decreases at depth. Depth-related changes in euphausiid eyes are considered with respect to the probable roles of vision and bioluminescence in the deep-sea. Unusual features of the eyes of several species are described.     

Where Are We Now? Bergmann's Rule Sensu Lato in Insects

Abstract Bergmann's rule states that individuals of a species/clade at higher altitudes or latitudes will be larger than those at lower ones. A systemic review of the known literature on inter- and intraspecific variation in insect size along latitudinal or altitudinal clines was done to see how often such clines appeared and whether they reflected classwide, species-specific, or experimentally biased tendencies. Nearly even numbers of studies showed Bergmann clines and converse-Bergmann clines, where insects get smaller as latitude/altitude increases. In fact, the majority of studies suggested no clines at all. Small ranges may have obscured certain clines, while giant ranges may have introduced artifacts. Researchers examining interspecific patterns found clines less frequently than those examining intraspecific patterns because of variation among species within the clades, which renders interspecific studies unhelpful. Bergmann's rule does not apply to hexapods with nearly the same consistency as it does to endothermic vertebrates. The validity of Bergmann's rule for any group and range of insects is highly idiosyncratic and partially depends on the study design. I conclude that studies of Bergmann's rule should focus within species and look at widespread but contiguous populations to account for all sources of variation while minimizing error.     

Wing trait–inversion associations in Drosophila subobscura can be generalized within continents,but may change through time

Clinal variation is one of the most emblematic examples of the action of natural selection at a wide geographical range. In Drosophila subobscura, parallel clines in body size and inversions, but not in wing shape, were found in Europe and South and North America. Previous work has shown that a bottleneck effect might be largely responsible for differences in wing trait–inversion association between one European and one South American population. One question still unaddressed is whether the associations found before are present across other populations of the European and South American clines. Another open question is whether evolutionary dynamics in a new environment can lead to relevant changes in wing traits–inversion association. To analyse geographical variation in these associations, we characterized three recently laboratory founded D. subobscura populations from both the European and South American latitudinal clines. To address temporal variation, we also characterized the association at a later generation in the European populations. We found that wing size and shape associations can be generalized across populations of the same continent, but may change through time for wing size. The observed temporal changes are probably due to changes in the genetic content of inversions, derived from adaptation to the new, laboratory environment. Finally, we show that it is not possible to predict clinal variation from intrapopulation associations. All in all this suggests that, at least in the present, wing traits–inversion associations are not responsible for the maintenance of the latitudinal clines in wing shape and size.     

Latitudinal insect body size clines revisited: a critical evaluation of the saw-tooth model

1.?Insect body size is predicted to increase with decreasing latitude because time available for growth increases. In insects with changing voltinism (i.e. number of generations per season), sharp decreases in development time and body size are expected at season lengths where new generations are added to the phenology of a species, giving rise to saw-tooth clines in these traits across latitudes. Growth rate variation may affect the magnitude of variation in body size or even reverse the saw-tooth cline. 2.?In this study, we analyse latitudinal body size clines in four geometrid moths with changing voltinism in a common laboratory environment. In addition to body size, we measured larval development time and growth rate and genetic correlations among the three traits. 3.?The patterns of clinal variation in body size were diverse, and the theory was not supported even when saw-tooth body size clines were found. Larval development time increased and growth rate decreased consistently with increasing season length, the clines in these traits being uniform. 4.?The consistencies of development time and growth rate clines suggest a common mechanism underlying the observations. Such a mechanism is discussed in relation to the complex interdependencies among the traits.     

Latitudinal clines in<Emphasis Type="Italic">Drosophila melanogaster</Emphasis>: Body size,allozyme frequencies,inversion frequencies,and the insulin-signalling pathway

Many latitudinal clines exist inDrosophila melanogaster: in adult body size, in allele frequency at allozyme loci, and in frequencies of common cosmopolitan inversions. The question is raised whether these latitudinal clines are causally related. This review aims to connect data from two very different fields of study, evolutionary biology and cell biology, in explaining such natural genetic variation inD. melanogaster body size and development time. It is argued that adult body size clines, inversion frequency clines, and clines in allele frequency at loci involved in glycolysis and glycogen storage are part of the same adaptive strategy. Selection pressure is expected to differ at opposite ends of the clines. At high latitudes, selection onD. melanogaster would favour high larval growth rate at low temperatures, and resource storage in adults to survive winter. At low latitudes selection would favour lower larval critical size to survive crowding, and increased male activity leading to high male reproductive success. Studies of the insulin-signalling pathway inD. melanogaster point to the involvement of this pathway in metabolism and adult body size. The genes involved in the insulin-signalling pathway are associated with common cosmopolitan inversions that show latitudinal clines. Each chromosome region connected with a large common cosmopolitan inversion possesses a gene of the insulin transmembrane complex, a gene of the intermediate pathway and a gene of the TOR branch. The hypothesis is presented that temperateD. melanogaster populations have a higher frequency of a ’thrifty’ genotype corresponding to high insulin level or high signal level, while tropical populations possess a more ’spendthrift’ genotype corresponding to low insulin or low signal level.     

Classic clover cline clues

Adaptive clines are striking examples of natural selection in action, yet few have been studied in depth. In this issue of Molecular Ecology, Kooyers & Olsen (2012) introduce modern analyses and thinking towards studies of a classical example of the rapid and repeated evolution of latitudinal and altitudinal clines in cyanogenesis in white clover, Trifolium repens L. Recognizing that adaptive clines represent trade-offs in the selective benefits of traits at different ends of a geographical transect, these researchers focus on whether evidence for selection can be found at regional (coarse) and local (fine) scales. After adjusting for population genetic patterns generated by demographic processes, Kooyers and Olsen provide evidence that the cyanogenesis cline is adaptive across a transect from Louisiana to Wisconsin, USA. Within local populations, divergent selection on coupling dominant and recessive alleles that underlie cyanogenesis is predicted to drive populations to gametic phase disequilibrium (LD), a pattern that has been found in several other studies reviewed by Kooyers and Olsen. The absence of LD within any sampled populations in this study leads the authors to suggest that selective patterns within these clines may be more complex than previously proposed, perhaps even following theoretical predictions of a geographic mosaic.     

A comparison of the genetic basis of wing size divergence in three parallel body size clines of Drosophila melanogaster

Body size clines in Drosophila melanogaster have been documented in both Australia and South America, and may exist in Southern Africa. We crossed flies from the northern and southern ends of each of these clines to produce F(1), F(2), and first backcross generations. Our analysis of generation means for wing area and wing length produced estimates of the additive, dominance, epistatic, and maternal effects underlying divergence within each cline. For both females and males of all three clines, the generation means were adequately described by these parameters, indicating that linkage and higher order interactions did not contribute significantly to wing size divergence. Marked differences were apparent between the clines in the occurrence and magnitude of the significant genetic parameters. No cline was adequately described by a simple additive-dominance model, and significant epistatic and maternal effects occurred in most, but not all, of the clines. Generation variances were also analyzed. Only one cline was described sufficiently by a simple additive variance model, indicating significant epistatic, maternal, or linkage effects in the remaining two clines. The diversity in genetic architecture of the clines suggests that natural selection has produced similar phenotypic divergence by different combinations of gene action and interaction.     

A hybrid zone comprising staggered chromosomal clines in the house mouse (Mus musculus domesticus).

In the vicinity of John o'Groats (Caithness, Scotland) there is a small karyotypic race of the house mouse (Mus musculus domesticus) characterized by a diploid number of 32 chromosomes, including the metacentrics 4.10, 9.12, 6.13 and 11.14. This race forms a hybrid zone with the standard British race (fully acrocentric chromosomes, 2n = 40). Although hybrid zones normally consist of several (or many) narrow character clines at the same position, this zone is unusual in that the chromosomal clines do not coincide. The cline for arm combination 11.14 is staggered relative to the 6.13 cline and both are separate from the clines for 4.10 and 9.12 (which may or may not coincide). A variety of explanations for the structure of the hybrid zone are discussed. It is possible that this may be a case of 'zonal raciation'.     

Are latitudinal clines in body size adaptive?

Body size of animals often increases with increasing latitude. These latitudinal clines in body size have interested biologists for over 150 years. However, the mechanisms that generate these clines in size are still unclear, though latitudinal gradients in temperature appear to play an important role. More importantly, many studies that examine latitudinal clines in body size and the mechanisms responsible for these clines use phenotypic data, confounding genetic (adaptive) and non‐genetic (plasticity) sources of variation. Yet, most of these studies make adaptive conclusions based on phenotypic measures of size. Here I show the dangers of making adaptive inferences from phenotypic measures of size. In addition, I use a specific form of plasticity in body size of ectotherms, called the temperature–size rule, to illustrate how confusion about genetic and non‐genetic contributions to phenotypic variation has hampered progress in understanding the evolution of latitudinal clines in size. Field‐based measurements of body size can no doubt be influenced by plasticity, but demonstrating that latitudinal clines have a genetic basis is necessary to show that these patterns are adaptive.     

A New Barrier to Dispersal Trapped Old Genetic Clines That Escaped the Easter Microplate Tension Zone of the Pacific Vent Mussels

Comparative phylogeography of deep-sea hydrothermal vent species has uncovered several genetic breaks between populations inhabiting northern and southern latitudes of the East Pacific Rise. However, the geographic width and position of genetic clines are variable among species. In this report, we further characterize the position and strength of barriers to gene flow between populations of the deep-sea vent mussel Bathymodiolus thermophilus. Eight allozyme loci and DNA sequences of four nuclear genes were added to previously published sequences of the cytochrome c oxidase subunit I gene. Our data confirm the presence of two barriers to gene flow, one located at the Easter Microplate (between 21°33′S and 31°S) recently described as a hybrid zone, and the second positioned between 7°25′S and 14°S with each affecting different loci. Coalescence analysis indicates a single vicariant event at the origin of divergence between clades for all nuclear loci, although the clines are now spatially discordant. We thus hypothesize that the Easter Microplate barrier has recently been relaxed after a long period of isolation and that some genetic clines have escaped the barrier and moved northward where they have subsequently been trapped by a reinforcing barrier to gene flow between 7°25′S and 14°S.     

The Size-Depth Relationship in Deep Ocean Animals

In response to Thiel's (1975). hypothesis that the food-limited deep sea is a small organism habitat, further data on average size of individuals representing various deep-sea taxa are presented. Our data were gathered with trawls and box corers between 200 and 5000 meters, in the western North Atlantic. For echinoderms, decapods and macrofauna there appears to be no steady, logarithmic decline in size with increasing depth, but fishes are bigger – deeper.     

Latitudinal pattern in body size in a cockroach,Eupolyphaga sinensis

Body size of insects with flexible life cycles is expected to conform to the saw‐tooth model, a model in which the relationship between size and developmental time depends on length of the growing season. In species with high variability in terms of voltinism, however, more complex patterns can be expected. Few empirical studies have demonstrated the existence of such relationships, or whether climatic factors contribute to these relationships. In this study, we investigated the geographic variation in body size of the Chinese cockroach, Eupolyphaga sinensis Walker (Blattaria: Polyphagidae), which has a variable life cycle length. The sizes of adults – collected from 14 localities ranging from temperate to subtropical zones in China – were measured, using body length, body width, and pronotum width as parameters. The relationship between size, latitude, and climate factors (encompassing 10 variables) was then investigated. We found that the body size of E. sinensis varied considerably with latitude: cockroaches were larger at low and high latitudes, but smaller at intermediate latitudes. Thus, the relationship between climate and body size conformed to a saw‐tooth pattern. Results indicate that two factors were significantly associated with body size clines: season length and variability in life cycle length. Our results also demonstrated that climatic factors contribute to latitudinal clines in body size, which has important ecological and evolutionary implications. It can be expected that global climate change may alter latitudinal clines in body size of E. sinensis.     

An interspecific test of Bergmann's rule reveals inconsistent body size patterns across several lineages of water beetles (Coleoptera: Dytiscidae)

1. Bergmann's rule sensu lato, the ecogeographic pattern relating animals' body size with environmental temperature (or latitude), has been shown to be inconsistent among insect taxa. Body size clines remain largely unexplored in aquatic insects, which may show contrasting patterns to those found in terrestrial groups because of the physiological or mechanical constraints of the aquatic environment. 2. Bergmann's rule was tested using data on body size, phylogeny and distribution for 93 species belonging to four lineages of dytiscid water beetles. The relationship between size and latitude was explored at two taxonomic resolutions – within each independent lineage, and for the whole dataset – employing phylogenetic generalised least‐squares to control for phylogenetic inertia. The potential influence of habitat preference (lotic versus lentic) on body size clines was also considered. 3. Within‐lineage analyses showed negative relationships (i.e. converse Bergmann's rule), but only in two lineages (specifically in those that included both lotic and lentic species). By contrast, no relationship was found between body size and latitude for the whole dataset. 4. These results suggest that there may be no universal interspecific trends in latitudinal variation of body size in aquatic insects, even among closely related groups, and show the need to account for phylogenetic inertia. Furthermore, habitat preferences should be considered when exploring latitudinal clines in body size in aquatic taxa at the interspecific level.     

Ambiguous species boundaries: Hybridization and morphological variation in two closely related Rubus species along altitudinal gradients

Although hybridization frequently occurs among plant species, hybrid zones of divergent lineages formed at species boundaries are less common and may not be apparent in later generations of hybrids with more parental‐like phenotypes, as a consequence of backcrossing. To determine the effects of dispersal and selection on species boundaries, we compared clines in leaf traits and molecular hybrid index along two hybrid zones on Yakushima Island, Japan, in which a temperate (Rubus palmatus) and subtropical (Rubus grayanus) species of wild raspberry are found. Leaf sinus depth in the two hybrid zones had narrower clines at 600 m a.s.l. than the molecular hybrid index and common garden tests confirmed that some leaf traits, including leaf sinus depth that is a major trait used in species identification, are genetically divergent between these closely related species. The sharp transition in leaf phenotypic traits compared to molecular markers indicated divergent selection pressure on the hybrid zone structure. We suggest that species boundaries based on neutral molecular data may differ from those based on observed morphological traits.     

What determines conformity to Bergmann's rule?

Aim  Bergmann's rule, the tendency of body size within species in bird and mammal populations to be positively correlated with latitude, is among the best known biogeographical generalizations. The factors behind such clines, however, are not well understood. Here we use a large data base of 79 mammalian carnivore species to examine the factors affecting latitudinal size clines.
Location  Worldwide.
Methods  We measured the skulls and teeth of carnivores in natural history museums, and calculated the amount of variation in size explained by latitude, supplementing our measurements with published data. We examined the effects of a number of variables on the tendency to show latitudinal clines.
Results  We found that geographical range and latitudinal extent are strongly related to size clines. Minimum temperatures across the range, net primary productivity and habitat diversity also have some, albeit much less, influence.
Main conclusions  We suggest that species with large geographical ranges are likely to encounter significant heterogeneity in those factors that influence body size, and are thus likely to exhibit size clines. However, the key factors that determine body size may not always operate along a latitudinal (or other geographical) cline, but be spatially linked to patches in the species range. One such important factor is likely to be food availability, which we show is a strong predictor of size in the brown bear ( Ursus arctos ) but is not associated with a latitudinal cline. We argue that the spatial distribution of key resources within the species range constitutes a significant predictor of carnivore body size.     

Adaptation and constraint in the evolution of Drosophila melanogaster wing shape

SUMMARY We have taken advantage of parallel instances of natural selection on body size in Drosophila melanogaster to investigate constraints and adaptation affecting wing shape. Using recently developed techniques for statistical shape analysis, we have examined variation in wing shape in similar body size clines on three continents. Gender-related shape differences were constant among all populations, suggesting that gender differences represent a developmental constraint on wing shape. In contrast, the underlying shape varied significantly between continents and shape change within each cline (i.e., between small and large body size populations) also varied between continents. Therefore, variation at these two levels presumably results from either drift or natural selection. Functional considerations suggest that shape variation between the continents is unlikely to be adaptive. However, cline-related shape change, which we show has a significant allometric component, may be adaptive. The overall range of wing shape variation, across a large range of wing size, is extremely small, and the possibility that wing shape is subject to stabilizing selection (or canalization) is discussed.     

Local climate determines intra‐ and interspecific variation in sexual size dimorphism in mountain grasshopper communities

The climate is often evoked to explain broad‐scale clines of body size, yet its involvement in the processes that generate size inequality in the two sexes (sexual size dimorphism) remains elusive. Here, we analyse climatic clines of sexual size dimorphism along a wide elevation gradient (i) among grasshopper species in a phylogenetically controlled scenario and (ii) within species differing in distribution and cold tolerance, to highlight patterns generated at different time scales, mainly evolutionary (among species or higher taxa) and ontogenetic or microevolutionary (within species). At the interspecific level, grasshoppers were slightly smaller and less dimorphic at high elevations. These clines were associated with gradients of precipitation and sun exposure, which are likely indicators of other factors that directly exert selective pressures, such as resource availability and conditions for effective thermoregulation. Within species, we found a positive effect of temperature and a negative effect of elevation on body size, especially on condition‐dependent measures of body size (total body length rather than hind femur length) and in species inhabiting the highest elevations. In spite of a certain degree of species‐specific variation, females tended to adjust their body size more often than males, suggesting that body size in females can evolve faster among species and can be more plastic or dependent on nutritional conditions within species living in adverse climates. Natural selection on female body size may therefore prevail over sexual selection on male body size in alpine environments, and abiotic factors may trigger consistent phenotypic patterns across taxonomic scales.     

Selection does not favor larger body size at lower temperature in a seed-feeding beetle

Body size of many animals increases with increasing latitude, a phenomenon known as Bergmann's rule (Bergmann clines). Latitudinal gradients in mean temperature are frequently assumed to be the underlying cause of this pattern because temperature covaries systematically with latitude, but whether and how temperature mediates selection on body size is unclear. To test the hypothesis that the "relative" advantage of being larger is greatest at cooler temperatures we compare the fitness of replicate lines of the seed beetle, Stator limbatus, for which body size was manipulated via artificial selection ("Large,"Control," and "Small" lines), when raised at low (22 degrees C) and high (34 degrees C) temperatures. Large-bodied beetles (Large lines) took the longest to develop but had the highest lifetime fecundity, and highest fitness (r(C)), at both low and high temperatures. However, the relative difference between the Large and Small lines did not change with temperature (replicate 2) or was greatest at high temperature (replicate 1), contrary to the prediction that the fitness advantage of being large relative to being small will decline with increasing temperature. Our results are consistent with two previous studies of this seed beetle, but inconsistent with prior studies that suggest that temperature-mediated selection on body size is a major contributor to the production of Bergmann clines. We conclude that other environmental and ecological variables that covary with latitude are more likely to produce the gradient in natural selection responsible for generating Bergmann clines.     

The commonness of rarity in a deep-sea taxon

The generality and drivers of rarity, defined along the axes of geographic range, population size and habitat specificity, have received considerable scientific attention for well over a century. Yet, studies that examine rarity holistically among these three attributes are limited, especially among invertebrate and marine taxa. The perceived paradox of deep-sea species, with often low population size but large geographic ranges, remains poorly resolved and understood. Here I assess seven forms of rarity and their drivers in deep-sea bivalves across the Atlantic Ocean. Rarity appears to be a common trait among deep-sea bivalves, with nearly 85% of the species exhibiting some form of rarity. Bivalves also showed a strong bimodal pattern of very common and very rare species. Geographic range, population size and habitat specificity were all heavily right skewed. Taxonomic superfamilies, body size, energy availability, temperature, depth and latitude, all significantly predicted geographic range, population size and habitat specificity. In a few cases, these patterns were counter to theoretical expectations. The drivers of rarity appear to be predictable from knowledge of the intrinsic biological and extrinsic environmental context of the species. These findings have major implications for deep-sea conversation, especially as anthropogenic threats are increasing.