Time‐limited environments affect the evolution of egg–body size allometry

Initial offspring size is a fundamental component of absolute growth rate, where large offspring will reach a given adult body size faster than smaller offspring. Yet, our knowledge regarding the coevolution between offspring and adult size is limited. In time‐constrained environments, organisms need to reproduce at a high rate and reach a reproductive size quickly. To rapidly attain a large adult body size, we hypothesize that, in seasonal habitats, large species are bound to having a large initial size, and consequently, the evolution of egg size will be tightly matched to that of body size, compared to less time‐limited systems. We tested this hypothesis in killifishes, and found a significantly steeper allometric relationship between egg and body sizes in annual, compared to nonannual species. We also found higher rates of evolution of egg and body size in annual compared to nonannual species. Our results suggest that time‐constrained environments impose strong selection on rapidly reaching a species‐specific body size, and reproduce at a high rate, which in turn imposes constraints on the evolution of egg sizes. In combination, these distinct selection pressures result in different relationships between egg and body size among species in time‐constrained versus permanent habitats.     

The complex drivers of thermal acclimation and breadth in ectotherms

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid‐latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.     

Testing the beneficial acclimation hypothesis and its alternatives for locomotor performance

The beneficial acclimation hypothesis (BAH) is controversial. While physiological work all but assumes that the BAH is true, recent studies have shown that support for the BAH is typically wanting. The latter have been criticized for assessing the benefits of developmental plasticity rather than acclimation. Here we examine the BAH within a strong inference framework for five congeneric species of ameronothroid oribatid mites that occupy marine to terrestrial habitats. We do so by assessing responses of maximum speed, optimum temperature, and performance breadth, measured from -10 degrees C to 35 degrees C, to four treatment temperatures (0 degrees , 5 degrees , 10 degrees , and 15 degrees C). We show that the BAH and its alternatives often make similar empirical predictions. Weak beneficial acclimation is characteristic of one of the more marine species. In the other two upper-shore and marine species, evidence exists for deleterious acclimation and the colder-is-better hypothesis. In the two fully terrestrial species, there is no plasticity. Lack of plasticity is beneficial when cue reliability is low or costs of plasticity are high, and the former seems plausible in terrestrial habitats. However, weak plasticity in the upper-shore/marine species and the absence of plasticity in the terrestrial species might also be a consequence of phylogenetic constraint.     

Habitat transitions alter the adaptive landscape and shape phenotypic evolution in needlefishes (Belonidae)

Habitat occupancy can have a profound influence on macroevolutionary dynamics, and a switch in major habitat type may alter the evolutionary trajectory of a lineage. In this study, we investigate how evolutionary transitions between marine and freshwater habitats affect macroevolutionary adaptive landscapes, using needlefishes (Belonidae) as a model system. We examined the evolution of body shape and size in marine and freshwater needlefishes and tested for phenotypic change in response to transitions between habitats. Using micro‐computed tomographic (µCT) scanning and geometric morphometrics, we quantified body shape, size, and vertebral counts of 31 belonid species. We then examined the pattern and tempo of body shape and size evolution using phylogenetic comparative methods. Our results show that transitions from marine to freshwater habitats have altered the adaptive landscape for needlefishes and expanded morphospace relative to marine taxa. We provide further evidence that freshwater taxa attain reduced sizes either through dwarfism (as inferred from axial skeletal reduction) or through developmental truncation (as inferred from axial skeletal loss). We propose that transitions to freshwater habitats produce morphological novelty in response to novel prey resources and changes in locomotor demands. We find that repeated invasions of different habitats have prompted predictable changes in morphology.     

Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae)

Habitat shifts are implicated as the cause of many vertebrate radiations, yet relatively few empirical studies quantify patterns of diversification following colonization of new habitats in fishes. The pufferfishes (family Tetraodon‐tidae) occur in several habitats, including coral reefs and freshwater, which are thought to provide ecological opportunity for adaptive radiation, and thus provide a unique system for testing the hypothesis that shifts to new habitats alter diversification rates. To test this hypothesis, we sequenced eight genes for 96 species of pufferfishes and closely related porcupine fishes, and added 19 species from sequences available in GenBank. We time‐calibrated the molecular phylogeny using three fossils, and performed several comparative analyses to test whether colonization of novel habitats led to shifts in the rate of speciation and body size evolution, central predictions of clades experiencing ecological adaptive radiation. Colonization of freshwater is associated with lower rates of cladogenesis in pufferfishes, although these lineages also exhibit accelerated rates of body size evolution. Increased rates of cladogenesis are associated with transitions to coral reefs, but reef lineages surprisingly exhibit significantly lower rates of body size evolution. These results suggest that ecological opportunity afforded by novel habitats may be limited for pufferfishes due to competition with other species, constraints relating to pufferfish life history and trophic ecology, and other factors.     

Effects of oceanic salinity on body condition in sea snakes

Since the transition from terrestrial to marine environments poses strong osmoregulatory and energetic challenges, temporal and spatial fluctuations in oceanic salinity might influence salt and water balance (and hence, body condition) in marine tetrapods. We assessed the effects of salinity on three species of sea snakes studied by mark-recapture in coral-reef habitats in the Neo-Caledonian Lagoon. These three species include one fully aquatic hydrophiine (Emydocephalus annulatus), one primarily aquatic laticaudine (Laticauda laticaudata), and one frequently terrestrial laticaudine (Laticauda saintgironsi). We explored how oceanic salinity affected the snakes' body condition across various temporal and spatial scales relevant to each species' ecology, using linear mixed models and multimodel inference. Mean annual salinity exerted a consistent and negative effect on the body condition of all three snake species. The most terrestrial taxon (L. saintgironsi) was sensitive to salinity over a short temporal scale, corresponding to the duration of a typical marine foraging trip for this species. In contrast, links between oceanic salinity and body condition in the fully aquatic E. annulatus and the highly aquatic L. laticaudata were strongest at a long-term (annual) scale. The sophisticated salt-excreting systems of sea snakes allow them to exploit marine environments, but do not completely overcome the osmoregulatory challenges posed by oceanic conditions. Future studies could usefully explore such effects in other secondarily marine taxa such as seabirds, turtles, and marine mammals.     

The Zoogeography of Mammalian Basal Metabolic Rate

Zoogeographical effects on the basal metabolic rate (BMR) of 487 mammal species were analyzed using conventional and phylogenetically independent ANCOVA. Minimal BMR variance occurred at a "constrained body mass" of 358 g, whereas maximum variance occurred at the smallest and largest body masses. Significant differences in BMR were identified for similar-sized mammals from the six terrestrial zoogeographical zones (Afrotropical, Australasian, Indomalayan, Nearctic, Neotropical, and Palearctic). Nearctic and Palearctic mammals had higher basal rates than their Afrotropical, Australasian, Indomalayan, and Neotropical counterparts. Desert mammals had lower basal rates than mesic mammals. The patterns were interpreted with a conceptual model describing geographical BMR variance in terms of the influence of latitudinal and zonal climate variability. Low and high basal rates were explained in unpredictable and predictable environments, respectively, especially in small mammals. The BMR of large mammals may be influenced in addition by mobility and predation constraints. Highly mobile mammals tend to have high BMRs that may somehow facilitate fast running speeds, whereas less mobile mammals are generally dietary specialists and are often armored. The model thus integrates physiological and ecological criteria and makes predictions concerning body size and life-history evolution, island effects, and locomotor energetics.     

Male-male competition and repeated evolution of terrestrial breeding in Atlantic Coastal Forest frogs*

Terrestrial breeding is a derived condition in frogs, with multiple transitions from an aquatic ancestor. Shifts in reproductive mode often involve changes in habitat use, and these are typically associated with diversification in body plans, with repeated transitions imposing similar selective pressures. We examine the diversification of reproductive modes, male and female body sizes, and sexual size dimorphism (SSD) in the Neotropical frog genera Cycloramphus and Zachaenus, both endemic to the Atlantic rainforest of Brazil. Species in this clade either breed in rocky streams (saxicolous) or in terrestrial environments, allowing us to investigate reproductive habitat shifts. We constructed a multilocus molecular phylogeny and inferred evolutionary histories of reproductive habitats, body sizes, and SSD. The common ancestor was small, saxicolous, and had low SSD. Terrestrial breeding evolved independently three times and we found a significant association between reproductive habitat and SSD, with shifts to terrestrial breeding evolving in correlation with decreases in male body size, but not female body size. Terrestrial breeding increases the availability of breeding sites and results in concealment of amplexus, egg-laying, and parental care, therefore reducing male-male competition at all stages of reproduction. We conclude that correlated evolution of terrestrial reproduction and small males is due to release from intense male-male competition that is typical of exposed saxicolous breeding.     

Global patterns of body size evolution are driven by precipitation in legless amphibians

Body size shapes ecological interactions across and within species, ultimately influencing the evolution of large‐scale biodiversity patterns. Therefore, macroecological studies of body size provide a link between spatial variation in selection regimes and the evolution of animal assemblages through space. Multiple hypotheses have been formulated to explain the evolution of spatial gradients of animal body size, predominantly driven by thermal (Bergmann's rule), humidity (‘water conservation hypothesis’) and resource constraints (‘resource rule’, ‘seasonality rule’) on physiological homeostasis. However, while integrative tests of all four hypotheses combined are needed, the focus of such empirical efforts needs to move beyond the traditional endotherm–ectotherm dichotomy, to instead interrogate the role that variation in lifestyles within major lineages (e.g. classes) play in creating neglected scenarios of selection via analyses of largely overlooked environment–body size interactions. Here, we test all four rules above using a global database spanning 99% of modern species of an entire Order of legless, predominantly underground‐dwelling amphibians (Gymnophiona, or caecilians). We found a consistent effect of increasing precipitation (and resource abundance) on body size reductions (supporting the water conservation hypothesis), while Bergmann's, the seasonality and resource rules are rejected. We argue that subterranean lifestyles minimize the effects of aboveground selection agents, making humidity a dominant selection pressure – aridity promotes larger body sizes that reduce risk of evaporative dehydration, while smaller sizes occur in wetter environments where dehydration constraints are relaxed. We discuss the links between these principles with the physiological constraints that may have influenced the tropically‐restricted global radiation of caecilians.     

So small, so loud: extremely high sound pressure level from a pygmy aquatic insect (Corixidae, Micronectinae)

To communicate at long range, animals have to produce intense but intelligible signals. This task might be difficult to achieve due to mechanical constraints, in particular relating to body size. Whilst the acoustic behaviour of large marine and terrestrial animals has been thoroughly studied, very little is known about the sound produced by small arthropods living in freshwater habitats. Here we analyse for the first time the calling song produced by the male of a small insect, the water boatman Micronecta scholtzi. The song is made of three distinct parts differing in their temporal and amplitude parameters, but not in their frequency content. Sound is produced at 78.9 (63.6-82.2) SPL rms re 2.10(-5) Pa with a peak at 99.2 (85.7-104.6) SPL re 2.10(-5) Pa estimated at a distance of one metre. This energy output is significant considering the small size of the insect. When scaled to body length and compared to 227 other acoustic species, the acoustic energy produced by M. scholtzi appears as an extreme value, outperforming marine and terrestrial mammal vocalisations. Such an extreme display may be interpreted as an exaggerated secondary sexual trait resulting from a runaway sexual selection without predation pressure.     

Post-settlement migratory behaviour and growth-related costs in two diadromous fish species, Galaxias maculatus and Galaxias brevipinnis

The physiological challenges incurred during the transition from sea to fresh water and the constraints they place on the rate at which the common galaxiid Galaxias maculatus and the climbing galaxiid Galaxias brevipinnis can migrate from marine to freshwater habitats were examined. The duration of the marine to freshwater transition, the relationship between post-settlement age (PSA) and standard length ( L _S) as a proxy for energetic costs incurred during settlement and the potential effects of estuary geomorphology on migratory behaviour was investigated. Rate of upstream migration after settlement was not uniform. Upstream migration rate was slowest directly after settlement and increased with increasing PSA and distance from the river mouth, indicating a delay in upstream migration by newly recruited galaxiids. L _s did not increase with age, at least within the first 21 days post settlement. These patterns were consistent for both species, in spite of differences in their life histories, across the recruitment season, despite seasonal variation in recruit size, and among estuaries with different properties. The results suggest that the timing and speed of migratory behaviour primarily reflect physiological constraints. Given the duration of residency of these species in estuaries, this study indicates that estuaries are critical transitional habitats for diadromous fishes during their migration from marine to freshwater habitats.     

Convergent evolution of the gut microbiome in marine carnivores

The gut microbiome can help the host adapt to a variety of environments and is affected by many factors. Marine carnivores have unique habitats in extreme environments. The question of whether marine habitats surpass phylogeny to drive the convergent evolution of the gut microbiome in marine carnivores remains unanswered. In the present study, we compared the gut microbiomes of 16 species from different habitats. Principal component analysis (PCA) and principal coordinate analysis (PCoA) separated three groups according to their gut microbiomes: marine carnivores, terrestrial carnivores, and terrestrial herbivores. The alpha diversity and niche breadth of the gut microbiome of marine carnivores were lower than those of the gut microbiome of terrestrial carnivores and terrestrial herbivores. The gut microbiome of marine carnivores harbored many marine microbiotas, including those belonging to the phyla Planctomycetes, Cyanobacteria, and Proteobacteria, and the genus Peptoclostridium. Collectively, these results revealed that marine habitats drive the convergent evolution of the gut microbiome of marine carnivores. This study provides a new perspective on the adaptive evolution of marine carnivores.     

Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages

The transmission stages of parasites are key determinants of parasite fitness, but they also incur huge mortality. Yet the selective forces shaping the sizes of transmission stages remain poorly understood. We ran a comparative analysis of interspecific variation in the size of transmission stages among 404 species of parasitic trematodes. There are two transmission steps requiring infective stages in the life cycle of trematodes: transmission from the definitive to the first intermediate (snail) host is achieved by eggs and/or the miracidia hatched from those eggs, and transmission from the first to the second intermediate host is achieved by free-swimming cercariae. The sizes of these stages are under strong phylogenetic constraints. Our results show that taxonomy explains >50% of the unaccounted variance in linear mixed models, with most of the variance occurring at the superfamily level. The models also demonstrated that mollusc size is positively associated with egg volume, miracidial volume and cercarial body volume, but not with the relative size of the cercarial tail. In species where they encyst on substrates, cercariae have significantly larger bodies than in species penetrating chordates, although the relative size of the cercarial tail of species using chordates as second intermediate hosts was larger than in other trematode species. Habitat also matters, with larger cercarial tails seen in freshwater trematodes than in marine ones, and larger miracidial volumes in freshwater species than in marine ones. Finally, the latitude (proxy for local temperature) at which the trematode species were collected had no effect on the sizes of transmission stages. We propose that resource availability within the snail host, the probability of contacting a host, and the density and viscosity of the water medium combine to select for different transmission stage sizes.     

Allometry and selection in a novel predator–prey system: Australian snakes and the invading cane toad

Because many organismal traits vary with body size, interactions between species can be affected by the respective body sizes of the participants. We focus on a novel predator–prey system involving an introduced, highly toxic anuran (the cane toad, Bufo marinus ) and native Australian snakes. The chance of a snake dying after ingesting a toad depends on the size of the snake and the size of the toad, and ultimately reflects the effect of four allometries: (1) physiological tolerance (the rate that physiological tolerance to toad toxin changes with snake size); (2) swallowing ability (the rate that maximal ingestible toad size (i.e. snake head size) increases with snake body size); (3) prey size (the rate that prey size taken by snakes increases with snake head size) and (4) toad toxicity (the rate that toxicity increases with toad size). We measured these allometries, and combined them to estimate the rate at which a snake's resistance changes with toad toxicity. The parotoid glands (and thus, toxicity) of toads increased disproportionately with toad size (i.e. relative to body size, larger toads were more toxic) but simultaneously, head size relative to body size (and thus, maximal ingestible prey size relative to predator size) declined with increasing body size in snakes. Thus, these two allometries tended to cancel each other out. Physiological tolerance to toxins did not vary with snake body size. The end result was that across snake species, mean adult body size did not affect vulnerability. Within species, however, smaller predators were more vulnerable, because the intraspecific rate of decrease in relative head size of snakes was steeper than the rate of increase in toxicity of toads. Thus, toad invasion may cause disproportionate mortality of juvenile snakes, and adults of the sex with smaller mean adult body sizes.     

Ecological context and the importance of body and gnathopod size for pairing success in two amphipod ecomorphs

Ecological context generates interspecific variation in mating behavior by imposing differential constraints on the action of sexual selection, but operation of these constraints in nature is not well understood. We used field and laboratory studies to examine the importance of body size and size of sexually dimorphic appendages, the gnathopods, for pairing success in two freshwater amphipod species within the Hyalella azteca species complex. We focused on a large-bodied species found in habitats where ecological factors tend to favor large body size, and a small-bodied species in habitats where small body size is favored by size-selective predation. A field study indicated that although male pairing success was greater for larger males in both species, pairing success increased throughout the range of variation in male size in the large species, whereas, in the small species, pairing success was low for smaller individuals, but roughly constant across intermediate to larger sizes. A laboratory mate choice experiment was consistent with the field study, finding that females of the large species exhibited a preference for larger males that was independent of absolute male size, but females of the small species were indifferent when choosing between males of intermediate to larger size. Species also differed in the direction of sexual size dimorphism in the field, with males being the larger sex in the large species but the smaller sex in the small species, a pattern consistent with the species differences in mate preference. Large gnathopod size relative to body size was associated with enhanced pairing success across all body sizes for the large species, but, in the small species, large gnathopod size enhanced pairing success only in smaller males. Species differences in mating behavior appear consistent with change driven by differing forms of the interaction between sexual and natural selection.     

Morphological adaptations to marine life in snakes

We investigated morphological adaptations to aquatic life within animals that exhibit a structurally simple, elongate body form, i.e., snakes. This linear body plan should impose different biomechanical constraints than the classical streamlined body shape associated with propulsion by fins, feet, or wings. Our measurements of general body shape of terrestrial, amphibious, and marine snakes (all from the same phylogenetic lineage, the Elapidae) show that seasnakes display specialized morphological attributes for life in water. Most notably, the cross‐sectional body shape is circular in terrestrial snakes but dorso‐ventrally elongated in seasnakes (due to a prominent ventral keel); amphibious species (sea kraits) exhibit an intermediate shape. The tail of amphibious and marine species (a major propulsive structure during swimming) is higher and thinner than in terrestrial snakes (i.e., paddle‐shaped) but shorter relative to body length. The evolution of a laterally compressed shape has been achieved by an increase in body height rather than a decrease in body width, possibly reflecting selection for more effective propulsive thrust, and for an ability to maintain hydrodynamic efficiency despite the minor bodily distension inevitably caused by prey items and developing offspring. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc     

Axial allometry in a neutrally buoyant environment: effects of the terrestrial‐aquatic transition on vertebral scaling

Ecological diversification into new environments presents new mechanical challenges for locomotion. An extreme example of this is the transition from a terrestrial to an aquatic lifestyle. Here, we examine the implications of life in a neutrally buoyant environment on adaptations of the axial skeleton to evolutionary increases in body size. On land, mammals must use their thoracolumbar vertebral column for body support against gravity and thus exhibit increasing stabilization of the trunk as body size increases. Conversely, in water, the role of the axial skeleton in body support is reduced, and, in aquatic mammals, the vertebral column functions primarily in locomotion. Therefore, we hypothesize that the allometric stabilization associated with increasing body size in terrestrial mammals will be minimized in secondarily aquatic mammals. We test this by comparing the scaling exponent (slope) of vertebral measures from 57 terrestrial species (23 felids, 34 bovids) to 23 semi‐aquatic species (pinnipeds), using phylogenetically corrected regressions. Terrestrial taxa meet predictions of allometric stabilization, with posterior vertebral column (lumbar region) shortening, increased vertebral height compared to width, and shorter, more disc‐shaped centra. In contrast, pinniped vertebral proportions (e.g. length, width, height) scale with isometry, and in some cases, centra even become more spool‐shaped with increasing size, suggesting increased flexibility. Our results demonstrate that evolution of a secondarily aquatic lifestyle has modified the mechanical constraints associated with evolutionary increases in body size, relative to terrestrial taxa.     

High summer temperature explains bill size variation in salt marsh sparrows

Physiological factors are rarely proposed to account for variation in the morphology of feeding structures. Recently, bird bills have been demonstrated to be important convective and radiant heat sinks. Larger bills have greater surface area than smaller bills and could serve as more effective thermoregulatory organs under hot conditions. The heat radiating function of bills should be more important in open habitats with little shade and stronger convective winds. Furthermore, as a means of dumping heat without increasing water loss through evaporation, bills might play a particularly important thermoregulatory role in heat loss in windy habitat where fresh water is limited. North American salt marshes provide a latitudinal gradient of relatively homogeneous habitat that is windy, open, and fresh‐water limited. To examine the potential role of thermoregulation in determining bill size variation among ten species or subspecies of tidal marsh sparrows, we plotted bill size against maximum summer and minimum winter temperatures. Bill surface areas increases with summer temperature, which explained 82–89% of the variance (depending upon sex) when we controlled for genus membership. Latitude alone predicted bill surface area much more poorly than summer temperature, and winter temperatures explained < 10% of the variance in winter bill size. Tidal marsh sparrow bill morphology may, to a large degree, reflect the role of the bill in expelling excess body heat in these unbuffered, fresh‐water‐limited environments. This new example of Allen's rule reaffirms the importance of physiological constraints on the evolution of vertebrate morphologies, even in bird bills, which have conventionally been considered as products of adaptation to foraging niche.     

THE EVOLUTION OF BODY SHAPE IN RESPONSE TO HABITAT: IS REPRODUCTIVE OUTPUT REDUCED IN FLAT LIZARDS?

Body size and shape are primary determinants of reproductive output in a variety of taxa, so selection favoring specific body sizes and shapes may, in turn, have a direct affect on reproductive output, and ultimately fitness. In reptiles, species that occupy rocky habitats are often flattened, a morphological character that aids locomotion and life on rocks, but which may constrain reproductive output by reducing the amount of abdominal space available to fill with eggs or offspring. Using 20 species of tropical skink from a wide range of habitats, we quantified habitat use, body height, body volume, and reproductive output, to determine whether the evolution of a flattened body was correlated with a reduction in abdominal volume, and, in turn, with reduced reproductive output. In this group of lizards, the occupation of rocky habitats has led (1) to the evolution of a flattened body, and this shift in body shape has (2) caused a reduction in abdominal volume. Despite this reduction in abdominal volume reproductive output was unaffected, as flatter species compensate by being more "full" of eggs. Thus, we demonstrate that morphological adaptation for enhanced performance in specific habitats did not cause a reduction in instantaneous reproductive output.     

Back to the sea: secondary marine organisms from a biogeographical perspective

Secondary marine organisms belong to groups of terrestrial ancestry which have recolonized marine habitats. Some of them are, to various degrees, still dependent on the terrestrial habitat where they originated, which imposes certain limits in the expansion of their distribution range. This makes them an ideal subject for historical reconstruction. Here I perform biogeographical analyses on the global distribution of 12 groups of land-dependent secondary marine plants and animals (mangrove trees, sea turtles, sea snakes, seabirds and seals). When all groups are taken together, species diversity shows a unique bimodal pattern for each hemisphere, with high values in cold-temperate and tropical regions, but low values in mid-latitude regions. None of the individual groups considered reaches its highest species concentration in mid-latitude regions. This is shown to be due to the existence of three different species assemblages, inhabiting the three species-rich latitudinal bands (northern cold-temperate, tropical, and southern cold-temperate), and intermixing to a limited degree in the species-poor mid-latitude bands. This is evidence that secondary marine organisms diversified independently in cold-temperate and tropical regions, and strongly suggests that colonization from terrestrial habitats took place independently in the three species-rich latitudinal bands. Different constraints in the terrestrial habitat of origin are put forward as evolutionary incentives for colonizing the sea: glaciation processes in cold regions and competition in tropical regions.