Molecular phylogeny of the gobioid fishes (Teleostei: Perciformes: Gobioidei)

The phylogeny of groups within Gobioidei is examined with molecular sequence data. Gobioidei is a speciose, morphologically diverse group of teleost fishes, most of which are small, benthic, and marine. Efforts to hypothesize relationships among the gobioid groups have been hampered by the prevalence of reductive evolution among goby species; such reduction can make identification of informative morphological characters particularly difficult. Gobies have been variously grouped into two to nine families, several with included subfamilies, but most existing taxonomies are not phylogenetic and few cladistic hypotheses of relationships among goby groups have been advanced. In this study, representatives of eight of the nine gobioid familes (Eleotridae, Odontobutidae, Xenisthmidae, Gobiidae, Kraemeriidae, Schindleriidae, Microdesmidae, and Ptereleotridae), selected to sample broadly from the range of goby diversity, were examined. Complete sequence from the mitochondrial ND1, ND2, and COI genes (3573 bp) was used in a cladistic parsimony analysis to hypothesize relationships among the gobioid groups. A single most parsimonious topology was obtained, with decay indices indicating strong support for most nodes. Major phylogenetic conclusions include that Xenisthmidae is part of Eleotridae, and Eleotridae is paraphyletic with respect to a clade composed of Gobiidae, Microdesmidae, Ptereleotridae, Kraemeriidae, and Schindleriidae. Within this five-family clade, two clades are recovered. One includes Gobionellinae, which is paraphyletic with respect to Kraemeriidae, Sicydiinae, Oxudercinae, and Amblyopinae. The other contains Gobiinae, also paraphyletic, and including Microdesmidae, Ptereleotridae, and Schindleriidae. Previous morphological evidence for goby groupings is discussed; the phylogenetic hypothesis indicates that the morphological reduction observed in many goby species has been derived several times independently.     

The brain ofRhyacichthys aspro (Rhyacichthyidae,Gobioidei)

Rhyacichthys aspro has one of the highest encephalization indices of the Gobioidei, at the level of the amphibiousPeriophthalmus (Gobiidae, Oxudercinae). This high encephalization can be explained by its adaptation to the turbulent waters of mountain torrents. The brain morphology is typical of a perciform fish and similar to that of a gobioid except in the form and size of the cerebellum. The quantitative analysis of the brain structures shows a large size of the olfactory centers, a small size of the visual centers (compared to those of other Gobioidei) and a very large size of the cerebellar centers (more than twice the size in other Gobioidei). The brain organization shows thatRhyacichthys aspro, although some of its brain structures are typically gobioid (tegmentum, medulla oblongata), is not a generalized gobioid, because of the high degree of its biological adaptation and the correlated large size of its cerebellum.     

Increased brain size in mammals is associated with size variations in gene families with cell signalling,chemotaxis and immune-related functions

Genomic determinants underlying increased encephalization across mammalian lineages are unknown. Whole genome comparisons have revealed large and frequent changes in the size of gene families, and it has been proposed that these variations could play a major role in shaping morphological and physiological differences among species. Using a genome-wide comparative approach, we examined changes in gene family size (GFS) and degree of encephalization in 39 fully sequenced mammalian species and found a significant over-representation of GFS variations in line with increased encephalization in mammals. We found that this relationship is not accounted for by known correlates of brain size such as maximum lifespan or body size and is not explained by phylogenetic relatedness. Genes involved in chemotaxis, immune regulation and cell signalling-related functions are significantly over-represented among those gene families most highly correlated with encephalization. Genes within these families are prominently expressed in the human brain, particularly the cortex, and organized in co-expression modules that display distinct temporal patterns of expression in the developing cortex. Our results suggest that changes in GFS associated with encephalization represent an evolutionary response to the specific functional requirements underlying increased brain size in mammals.     

Energy metabolism, brain size and longevity in mammals

The mathematical relations between basal energy metabolism, brain size, and life span in mammals have been investigated. The evolutionary level of brain development, or encephalization (c), is a function both of brain weight (E) and of body weight (P) according to (formula; see text) Brain weight was found to be a linear function of the product of encephalization and basal metabolic rate. The oxygen consumption of the brain (Mbrain) is proportional to both encephalization and body weight according to (formula; see text) The ratio of metabolic rate in the cerebral cortex to that in the brain as a whole depends solely upon the degree of encephalization and is independent of the size of the animal. The maximum potential life span of a mammal was found to be proportional to the product of its degree of encephalization and the reciprocal of its metabolic rate per unit weight. Life span may be regarded as the algebraic sum of two components: (1) a deduced somatic component (Lb) inversely related to the basal metabolic rate per unit weight, and (2) an encephalization component (Le) related directly to the evolutionary increase of relative brain size.     

The brain organization of butterflyfishes

Synopsis The encephalization indices of angelfishes (Pomacanthidae) and butterflyfishes (Chaetodontidae) are typical of advanced perciform fishes: both families lie in the upper part of the polygon of teleost indices. The chaetodontids seem to be a little more encephalized than pomacanthids. The general morphology of the brains in both families is very similar: small olfactory bulbs, large optic tectum and a cerebellum which covers the brain structures in front of it like a cap. This morphology is shared by another family of the coral reef biotope, the Acanthuridae. The histological architecture is also typical of advanced teleosts, with a cortex-like pallium, a laminated nucleus geniculatus (= pretectalis superficialis), a complex valvula cerebelli and a corpus glomerulosum with a clear neuropile centre. The quantitative analysis of the main subdivisions of the brain, either from relative volumes or from indices, shows small olfactory bulbs (microsmy) but important telencephalic and diencephalic centres, large tectal centres (vision) and large cerebellum (precise locomotion). Many of these peculiarities are shared by other fishes inhabiting coral reefs. The differences between the two families seem to be primarily correlated with food habits: the angelfishes, which are sponge-feeders and may have an overweight due to the ballast of the sponge-skeleton in their digestive tract, and which do not need either such good vision or such precise locomotion to pick up their prey, could be a little less encephalized than the butterflyfishes.     

Life in the unthinking depths: energetic constraints on encephalization in marine fishes

Several hypotheses have been proposed to explain the limitation of brain size in vertebrates. Here, we test three hypotheses of brain size evolution using marine teleost fishes: the direct metabolic constraints hypothesis (DMCH), the expensive tissue hypothesis and the temperature‐dependent hypothesis. Our analyses indicate that there is a robust positive correlation between encephalization and basal metabolic rate (BMR) that spans the full range of depths occupied by teleosts from the epipelagic (< 200 m), mesopelagic (200–1000 m) and bathypelagic (> 4000 m). Our results disentangle the effects of temperature and metabolic rate on teleost brain size evolution, supporting the DMCH. Our results agree with previous findings that teleost brain size decreases with depth; however, we also recover a negative correlation between trophic level and encephalization within the mesopelagic zone, a result that runs counter to the expectations of the expensive tissue hypothesis. We hypothesize that mesopelagic fishes at lower trophic levels may be investing more in neural tissue related to the detection of small prey items in a low‐light environment. We recommend that comparative encephalization studies control for BMR in addition to controlling for body size and phylogeny.     

Reproductive strategies,body size,and encephalization in primate evolution

In order to understand fully the generally high level of encephalization observed in living primates, we must determine why early primates exhibited moderately large relative brain sizes compared to their early Tertiary contemporaries. The relatively high degree of encephalization in early primates may be related at least in part to the fact that they were highly unusualamong mammals in combining a small body size with a strongly precocial reporductive strategy. Other small, precocial mammals also exhibit moderately high levels of encephalization; but primates appear to have been truly uniquein being the only such small-sized and highly precocial group to give rise to extensive radiations of larger descendants. This is a key element in understanding primate brain evolution, because the initial “head start” of the early primates was translated up to larger sizes in descendants. The possible relationships among encephalization, precociality, small size, and arboreality are discussed, particularly in light of recent debates concerning the validity of the superorder Archonta. This work emphasizes that we need to consider relative brain size as but one element in a complex synergistic network of morphological and life-history features.     

Encephalization of Bathyergidae and comparison of brain structure volumes between the Zambian mole-rat Fukomys anselli and the giant mole-rat Fukomys mechowii

Encephalization indices were calculated for Fukomys anselli and Fukomys mechowii by using interspecific allometric lines of Tenrecinae (recent Eutheria with the smallest brains) and average Rodentia to compare brain sizes independent of body size influence. These were contrasted with corresponding indices of other Bathyergidae and additionally with other rodents. The Bathyergidae species had indices within the variation of some Cricetidae and Muridae and thus do not differ in encephalization. F. anselli, however, had a clearly higher encephalization index than the sister species F. mechowii. The sizes of diverse structures were measured in the brains of these two species by help of the serial section method. No differences were found in relative composition. The lower encephalization of F. mechowii is discussed as a special phenomenon of gigantism during phylogenetic radiation which similarly was documented for other forms.     

Early hominid body weight and encephalization

The body weight of the Plio-Pleistocene hominids of Africa is estimated by predicting equations derived from the Terry Collection of human skeletons with known body weights. About 50% of the variance in body weight can be accounted for by vertebral and femoral size. Predicted early hominid weights range from 27.6 kg (61 lb) to 54.3 kg (119 lb). The average weight for Australopithecus is 43.2 kg (95 lb) and for Homo sp. indet. from East Rudolf, Kenya, is 52.8 kg (116 lb). These estimates are consistent even if pongid proportions are assumed. Indices of encephalization show that the brain to body weight ratio in Australopithecus is above the great ape averages but well below Homo sapiens. The Homo sp. indet. represented by the KNM-ER 1470, O.H. 7 and O.H. 13 crania have encephalization indices above Australopithecus despite the greater body weight of the former.     

Dietary quality and encephalization in platyrrhine primates

The high energetic costs of building and maintaining large brains are thought to constrain encephalization. The 'expensive-tissue hypothesis' (ETH) proposes that primates (especially humans) overcame this constraint through reduction of another metabolically expensive tissue, the gastrointestinal tract. Small guts characterize animals specializing on easily digestible diets. Thus, the hypothesis may be tested via the relationship between brain size and diet quality. Platyrrhine primates present an interesting test case, as they are more variably encephalized than other extant primate clades (excluding Hominoidea). We find a high degree of phylogenetic signal in the data for diet quality, endocranial volume and body size. Controlling for phylogenetic effects, we find no significant correlation between relative diet quality and relative endocranial volume. Thus, diet quality fails to account for differences in platyrrhine encephalization. One taxon, in particular, Brachyteles, violates predictions made by ETH in having a large brain and low-quality diet. Dietary reconstructions of stem platyrrhines further indicate that a relatively high-quality diet was probably in place prior to increases in encephalization. Therefore, it is unlikely that a shift in diet quality was a primary constraint release for encephalization in platyrrhines and, by extrapolation, humans.     

Does encephalization correlate with life history or metabolic rate in Carnivora?

A recent analysis of brain size evolution reconstructed the plesiomorphic brain–body size allometry for the mammalian order Carnivora, providing an important reference frame for comparative analyses of encephalization (brain volume scaled to body mass). I performed phylogenetically corrected regressions to remove the effects of body mass, calculating correlations between residual values of encephalization with basal metabolic rate (BMR) and six life-history variables (gestation time, neonatal mass, weaning time, weaning mass, litter size, litters per year). No significant correlations were recovered between encephalization and any life-history variable or BMR, arguing against hypotheses relating encephalization to maternal energetic investment. However, after correcting for clade-specific adaptations, I recovered significant correlations for several variables, and further analysis revealed a conserved carnivoran reproductive strategy, linking degree of encephalization to the well-documented mammalian life-history trade-off between neonatal mass and litter size. This strategy of fewer, larger offspring correlating with increased encephalization remains intact even after independent changes in encephalization allometries in the evolutionary history of this clade.     

Species and shape diversification are inversely correlated among gobies and cardinalfishes (Teleostei: Gobiiformes)

Gobies and their relatives are significant components of nearshore marine, estuarine, and freshwater fish faunas in both tropical and temperate habitats worldwide. They are remarkable for their ability to adapt to and diversify in a wide range of environments. Among gobiiform clades, species diversities vary widely, ranging from two species in Kurtidae to more than 1,000 species in Gobiidae. There is also great variation in head and body shape and in environmental preferences (fresh, brackish, or marine habitats). In this study, I used a time-calibrated molecular phylogeny, coupled with morphometric and comparative analyses, to examine evolutionary rates of both speciation and morphological diversification among gobiiform lineages. Projection of the phylogeny onto a shape-derived morphospace shows that Gobioidei is morphometrically distinct from its sister taxon Apogonoidei, but that families within Gobioidei overlap in morphospace. Analysis of species diversification rates indicates that three rate shifts have occurred over the evolutionary history of Gobiiformes. Relative to the other lineages, Kurtidae has exhibited a slowdown in speciation, whereas both Apogonidae and Gobiidae?+?Gobionellidae have experienced an increase in diversification. Comparative analyses show that in Apogonidae and Gobiidae?+?Gobionellidae, increased speciation is correlated with diminished rates of morphological diversification, differently manifested in either clade and among the various sublineages. The elevation in speciation rates and diminishment in rates of morphological change in both Apogonidae and the clade Gobiidae?+?Gobionellidae are correlated with shifts to oceanic habitats from freshwater. This pattern is the complement to that seen across the global radiation of acanthomorph fishes in which a decrease in species diversification is associated with an increase in morphological disparity.     

Endocranial Volume of Mid-Late Eocene Archaeocetes (Order: Cetacea) Revealed by Computed Tomography: Implications for Cetacean Brain Evolution

The large brain of modern cetaceans has engendered much hypothesizing about both the intelligence of cetaceans (dolphins, whales, and porpoises) and the factors related to the evolution of such large brains. Despite much interest in cetacean brain evolution, until recently there have been few estimates of brain mass and/or brain–body weight ratios in fossil cetaceans. In the present study, computed tomography (CT) was used to visualize and estimate endocranial volume, as well as to calculate level of encephalization, for two fully aquatic mid-late Eocene archaeocete species, Dorudon atrox and Zygorhiza kochii. The specific objective was to address more accurately and more conclusively the question of whether relative brain size in fully aquatic archaeocetes was greater than that of their hypothesized sister taxon Mesonychia. The findings suggest that there was no increase in encephalization between Mesonychia and these archaeocete species.     

Fecundity of two hillstream fishes, Garra lamta (Ham.) and Garra gotyla gotyla (gray)

The fecundity of two hillstream fishes, Garra lamta and G. gotyla gotyla, is related to their total body length (L), total body weight (W), ovary length (X) and ovary weight (V). The relationships to L, W, X and V were all linear. The correlation coefficient values (r) showed that total body length and total body weight were the best indices in fecundity estimates in both fishes.     

The relative gonadal index: an alternative index for quantification of reproductive condition

Gonadal indices (i.e. GSI = gonadal wt/body wt X 100) commonly are used to quantify reproductive condition in fishes. These indices may be inappropriate with specimens of different sizes, however, for gonadal growth often is allometric. A new gonadal index (relative gonadal index, RGI) was developed to quantify the reproductive condition of animals independent of body size. The RGI is based on the underlying model W = alpha i X S beta i, where W is gonadal weight, S is body size (less gonadal weight if body weight is used), and alpha i and beta i are parameters to be estimated for gonadal developmental stage i. Assuming that a multiplicative lognormal error is appropriate, parameter estimates for alpha i and beta i were obtained by linear least squares regression for the log-transformed model ln(W) = beta i X ln(S) + ln(alpha i), where, in this form, beta i is the slope and ln(alpha i) is the intercept. Only if estimates of beta i do not differ significantly among ovarian developmental stages, as in our case, can a pooled estimate of beta be used to obtain the relative gonadal index, RGI = alpha i = W/S beta. Applicability of the RGI was tested using ovaries of three ecologically distinct fish species. The RGI was found to be more appropriate than the gonosomatic index for all three species.     

Brain morphology in large pelagic fishes: a comparison between sharks and teleosts

A quantitative comparison was made of both relative brain size (encephalization) and the relative development of five brain area of pelagic sharks and teleosts. Two integration areas (the telencephalon and the corpus cerebellum) and three sensory brain areas (the olfactory bulbs, optic tectum and octavolateralis area, which receive primary projections from the olfactory epithelium, eye and octavolateralis senses, respectively), in four species of pelagic shark and six species of pelagic teleost were investigated. The relative proportions of the three sensory brain areas were assessed as a proportion of the total 'sensory brain', while the two integration areas were assessed relative to the sensory brain. The allometric analysis of relative brain size revealed that pelagic sharks had larger brains than pelagic teleosts. The volume of the telencephalon was significantly larger in the sharks, while the corpus cerebellum was also larger and more heavily foliated in these animals. There were also significant differences in the relative development of the sensory brain areas between the two groups, with the sharks having larger olfactory bulbs and octavolateralis areas, whilst the teleosts had larger optic tecta. Cluster analysis performed on the sensory brain areas data confirmed the differences in the composition of the sensory brain in sharks and teleosts and indicated that these two groups of pelagic fishes had evolved different sensory strategies to cope with the demands of life in the open ocean.     

Body Weight and Relative Brain Size (Encephalization) in Eocene Archaeoceti (Cetacea)

Calibration of the Brownian diffusion model of Felsenstein indicates that phylogeny may have an influence on body length and other phenotypic measures in Cetacea for as many as 10,000 generations or about 180,000 years, which is negligible in the 35 million year history of extant Cetacea. Observations of phenotypic traits in cetacean species living today are independent of phylogeny and independent statistically. Four methods for estimating body weight in fossil cetaceans are compared: (1) median serial regression involving a set of multiple regressions of log body weight on log centrum length, width, and height for core vertebrae; (2) regression of log whole body weight on log body length for individuals; (3) regression of log whole body weight on log body length for species means; and (4) regression of log lean body weight on log body length for individuals. These yield body weight estimates for the Eocene archaeocete Dorudon atrox of 1126, 1118, 1132, and 847 kg, respectively, with consistency and applicability to partial skeletons favoring the first approach. The whole-body weight expected, P_e (in kg), for a given body length, L_i (in cm), is given by log₁₀ P_e?=?2.784 ? log₁₀ L_i???4.429. Negative allometry of body weight and body length (slope 2.784?<?3.000) means that small cetaceans are shorter and more maneuverable than expected for their weight, while large cetaceans are longer and more efficient energetically than expected for their weight. Encephalization is necessarily quantified relative to a reference sample, most mammals are terrestrial, and terrestrial mammals provide a logical baseline. The encephalization residual for living terrestrial mammals as a class (ER_TC), is the difference between observed log₂ brain weight (E_i in g) and expected log₂ brain weight (E_e in g), where the latter is estimated from body weight (P_i in g), as log₂ E_e?=?0.740 ? log₂ P_i???4.004. ER_TC is positive for brains that are larger than expected for a given body size, and negative for brains that are smaller than expected. Base-2 logarithms make the ER_TC scale intuitive, in uniform units of halving or doubling. Encephalization quotients (EQ) are unsuitable for comparison because they are proportions on a non-uniform scale. Middle Eocene archaeocetes have ER_TC values close to ?2 (two halvings compared to expectation), while late Eocene archaeocetes have ER_TC values close to ?1 (one halving compared to expectation). ER_TC is not known for fossil mysticetes, but living mysticetes have ER_TC values averaging about ?2. Oligocene-Recent odontocetes appear to have ER_TC values averaging about +1 (one doubling compared to expectation) through their temporal range. Definitive interpretation of the evolution of encephalization in Cetacea will require better documentation for Oligocene–Recent mysticetes and odontocetes.     

The regularities in connection between fecundity with body weight and growth rate in fishes

The absolute and relative fecundity of freshwater, anadromous and marine fishes (102 species and subspecies from 33 families) and its dependence on body mass and growth rate were analyzed on the basis of published data. According to the spawning type all studied fishes were divided into species with short-term and single spawning and fishes with extended or long-term spawning. The equations of dependence of absolute fecundity (E) on body mass (W) were calculated: E = 1.033 W0.578 (the first group) and E = 0.792 W0.74 (the second group). If W < 177 g the equations don't differ significantly and one may use the equation E = 1.34(-0.742) for both groups. The body mass of females at age of maturity expressed as a portion of maximal definitive body mass equals 0.22 +/- 0.044 for many different species with 0.95 probability. The relative fecundity (a1) of some species negatively correlates with maximal body mass of adult individuals (Wmax). This dependence is expressed by equations: a1 = 3.033 Wmax-0.549 (for the first group) and a1 = 1.726 Wmax-0.351 (for the second group). Value of ratio Wov/W of different fish species changes irregularly from 0.054 to 0.32 and its average is 0.150 +/- 0.012 for the first group and 0.156 +/- 0.007 for the second one. In such a way, single reproduction effort of fishes is approximately 0.15. Comparison of data on Pisces, Crustacea, Amphibia, Reptilia, and Mammalia revealed that reproduction effort of different aquatic and terrestrial invertebrates and vertebrates varies within rather narrow limits (from 0.05 to 0.44). Average values of this index varies even less--from 0.097 to 0.238, on average 0.162, i.e. approximately 15-18% of animals' body mass falls on their reproduction constituent.     

Neuroecology of cartilaginous fishes: the functional implications of brain scaling

It is a widely accepted view that neural development can reflect morphological adaptations and sensory specializations. The aim of this review is to give a broad overview of the current status of brain data available for cartilaginous fishes and examine how perspectives on allometric scaling of brain size across this group of fishes has changed within the last 50 years with the addition of new data and more rigorous statistical analyses. The current knowledge of neuroanatomy in cartilaginous fishes is reviewed and data on brain size (encephalization, n = 151) and interspecific variation in brain organization (n = 84) has been explored to ascertain scaling relationships across this clade. It is determined whether similar patterns of brain organization, termed cerebrotypes, exist in species that share certain lifestyle characteristics. Clear patterns of brain organization exist across cartilaginous fishes, irrespective of phylogenetic grouping and, although this study was not a functional analysis, it provides further evidence that chondrichthyan brain structures might have developed in conjunction with specific behaviours or enhanced cognitive capabilities. Larger brains, with well-developed telencephala and large, highly foliated cerebella are reported in species that occupy complex reef or oceanic habitats, potentially identifying a reef-associated cerebrotype. In contrast, benthic and benthopelagic demersal species comprise the group with the smallest brains, with a relatively reduced telencephalon and a smooth cerebellar corpus. There is also evidence herein of a bathyal cerebrotype; deep-sea benthopelagic sharks possess relatively small brains and show a clear relative hypertrophy of the medulla oblongata. Despite the patterns observed and documented, significant gaps in the literature have been highlighted. Brain mass data are only currently available on c. 16% of all chondrichthyan species, and only 8% of species have data available on their brain organization, with far less on subsections of major brain areas that receive distinct sensory input. The interspecific variability in brain organization further stresses the importance of performing functional studies on a greater range of species. Only an expansive data set, comprised of species that span a variety of habitats and taxonomic groups, with widely disparate behavioural repertoires, combined with further functional analyses, will help shed light on the extent to which chondrichthyan brains have evolved as a consequence of behaviour, habitat and lifestyle in addition to phylogeny.     

Problems of body-weight estimation in fossil primates

Body-weight estimates of fossil primates are commonly used to infer many important aspects of primate paleobiology, including diet, ecology, and relative encephalization. It is important to examine carefully the methodologies and problems associated with such estimates and the degree to which one can have confidence in them. New regression equations for predicting body weight in fossil primates are given which provide body-weight estimates for most nonhominid primate species in the fossil record. The consequences of using different subgroups (evolutionary “grades”) of primate species to estimate fossil-primate body weights are explored and the implications of these results for interpreting the primate fossil record are discussed. All species (fossil and extant) were separated into the following “grades”: prosimian grade, monkey grade, ape grade, anthropoid grade, and all-primates grade. Regression equations relating lower molar size to body weight for each of these grades were then calculated. In addition, a female-anthropoid grade regression was also calculated for predicting body weight infernales of extinct, sexually dimorphic anthropoid species. These equations were then used to generate the fossil-primate body weights. In many instances, the predicted fossil-primate body weights differ substantially from previous estimates.