ALLOMETRIC CONSTRAINTS AND THE EVOLUTION OF ALLOMETRY

Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than 300 empirical estimates of static (within‐species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million‐year, cross‐species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait–size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow‐sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable.     

Karl Ernst Ritter von Baer

The discoverer of the egg‐cell: Karl Ernst von Baer Being a versatile scientist of great influence, the Baltic aristocrat Karl Ernst von Baer (1792–1876) became the originator of comparative ontogeny. During his time as professor at Königsberg University von Baer, who formerly studied medicine, developed a deep interest in processes of recapitulation during embryonic growth and discovered the spinal cord and the mammalian egg‐cell. After retirement he became one of the most prominent opponents of Charles Darwin. Von Baer established several scientific laws, societies and journals.     

CONVERGENT EVOLUTION IN INVERTEBRATES

Resemblance between animal taxa may be due to convergence rather than to recent common ancestry. Constraints on biological materials and adaptation to particular habits or habitats will produce widespread convergence. How may we distinguish the two causes of resemblance? The relationship between convergence and taxonomy is discussed, demonstrating that the choice of taxonomic method will itself determine the extent to which convergence is perceived. In particular, cladistic analysis based on parsimony will tend to minimise and thus conceal convergence: neither the resulting cladogram nor a consistency index derived from it can be used to assess the prevalence of convergence. With any taxonomic system, there can be no substitute for evaluation of the morphological characters used. Complementary use of molecular characters shows promise: we wait further understanding of constraints in genetic evolution and of the possibilities of convergence at this level also. These general principles are illustrated with a range of examples from within and between invertebrate phyla: the phylogeny of Cnidaria and Platyhelminthes cannot be traced with certainty, but where the fossil record allows clear rooting, as for the echinoderms and in particular the echinoids, combination of morphological and molecular methods has made much progress. Sub-groups within a phylum, for example opisthobranch molluscs and the dipteran Phoridae, may show an uncontested phylogeny, and here studies have precisely identified convergence and shown that it may be the commoner cause of resemblance. Adaptation to exacting environments shown by terrestial and freshwater nemertines may also result in a predominance of convergent resemblance. Traditional grouping of phyla breaks down on re-examination of supposedly key characters, such as segmentation, body cavities, germ layers and symmetry, each of which must have had multiple origins: nor are developmental stages (especially not larvae) a reliable guide to relationships. Demarcation of phyla may be difficult, as with arthropods, and location of phyla is even more difficult, due to their early and rapid radiation. Over-simplified definition of characters has bedevilled invertebrate classification and the use of molecular data has not yet resolved the major controversies. The question ‘How common is convergence?’ remains unanswered and may be unanswerable. Our examples indicate that even the minimum detectable levels of convergence are often high, and we conclude that at all levels convergence has been greatly underestimated.     

Allometric and trait‐based patterns in parasite stoichiometry

We measured the elemental content (%C, N and P) and ratios (C:N, C:P, N:P) of a diverse assemblage of parasitic helminths to ask whether taxonomy or traits were related to stoichiometric variation among species. We sampled 27 macroparasite taxa, spanning four phyla, infecting vertebrate and invertebrate hosts from freshwater ecosystems in New Jersey. Macroparasites varied widely in elemental content, exhibiting 4.7‐fold variation in %N, 4.6‐fold variation in %P, and 11.5‐fold variation in N:P. Across all species, parasite %P scaled negatively and C:P scaled positively with body size. Similar relationships between parasite P content and body size occurred at the phylum level and within individual species. The allometric scaling of P across species supports the growth rate hypothesis, which predicts that smaller taxa require more P to support relatively higher growth rates. Life cycle stage was related to %N and C:N, with non‐reproductive parasite stages lower in %N and higher in C:N than actively reproducing parasites. Parasite phylum, functional feeding group, and trophic level did not explain elemental variation among species. Organismal stoichiometry is linked to ecological function, and wide variation in macroparasite stoichiometry likely generates diverse patterns in host–parasite nutrient dynamics and variable relationships between parasitism and nutrient cycling.     

THE MOLLUSCAN RHOGOCYTE (PORE-CELL, BLASENZELLE, CELLULE NUCALE), AND ITS SIGNIFICANCE FOR IDEAS ON NEPHRIDIAL EVOLUTION

The rhogocyte (Leydig's cell, cellule nucale, Blasen-zelle,pore cell) is a specific molluscan cell type that occurs throughoutthe animal's primary body cavity, i.e free in the haemocoelor embedded in connective tissue. Rhogocytes closely resemblecyrtocytes and podocytes jn having slit-Uke diaphragms withan encoating extracellular matrix at their surface which probablyacts as a molecular sieve However, rhogocytes are solitary cells,whereas cyrtocytes and podocytes form epitheha Occurrence, variability,naming, and possible functions of the rhogocyte among the MoUuscaare reviewed and discussed. In general, rhogocytes play an importantrole in metal ion metabolism of molluscs, they are possiblyinvolved in the recycling of respiratory pigments and may alsoact in detoxification. Up to now direct homologues of the molluscan rhogocyte havenot been described in any other bi-laterian phylum, so-called‘pore cells’ of other phyla show entirely differentfine-structures However, at least partial (serial) homologycan be accepted between rhogocytes (free cells), arthropod nephro-cytes(cell aggregates or solitary cells) and podocytes (true epithelialcells), and there is also a cytological and functional continuumof both rhogocytes and podocytes to protonephndial cyrto- respectivelysolenocytes. Implications of this postulated ‘cell-family’with slit-diaphragms and their respective ultrafiltration systemsfor theories on the evolution of filtration nephndia are discussed. (Received 10 February 1995; accepted 10 October 1995)     

Allometry and chromosomal speciation of the casiraguas Proechimys (Mammalia, Rodentia)

Morphometric characters (linear measurements) of the skull and mandible of the rodent Proechimys occurring in Venezuela and Columbia were investigated through multivariate techniques in order to describe static allometry and to relate allometric patterns to the recent evolution of these taxa. At least five species originated during the recent Pleistocene period in the upper Orinoco basin, all characterized by different karyotypes, one of them (P. guairae) being a Rassenkreis of karyomorphs. Species are characterized by unique static allometric patterns and the study of these patterns suggests a phylogenetic rather than an ecogenetic origin for these patterns; modifications in the shape of the skull and the mandible have originated during phyletic speciation and there is no apparent sign of functional adaptation.     

Cope's rule in cryptodiran turtles: do the body sizes of extant species reflect a trend of phyletic size increase?

Cope's rule of phyletic size increase is questioned as a general pattern of body size evolution. Most studies of Cope's rule have examined trends in the paleontological record. However, neontological approaches are now possible due to the development of model-based comparative methods, as well as the availability of an abundance of phylogenetic data. I examined whether the phylogenetic distribution of body sizes in extant cryptodiran turtles is consistent with Cope's rule. To do this, I examined body size evolution in each of six major clades of cryptodiran turtles and also across the whole tree of cryptodirans (n = 201 taxa). Extant cryptodiran turtles do not appear to follow Cope's rule, as no clade showed a significant phyletic body size trend. Previous analyses in other extant vertebrates have also found no evidence for phyletic size increase, which is in contrast to the paleontological data that support the rule in a number of extinct vertebrate taxa.     

ON PHENOTYPIC EXPRESSION,MORPHOGENETIC PATTERN AND SYNANGIUM EVOLUTION IN PSILOTUM

Both the typical form and the appendageless variant of Psilotum nudum produce terminal synangia at the ultimate tips of the aerial axes. One clone in particular of the typical appendaged form produced synangia entirely at the tips of the aerial branches, as in the appendageless variant, and also developed occasional lateral transitional entities on the upper aerial axis displaying appendagelike and axislike morphological qualities. A developmental comparison of synangium development at the ultimate tips of aerial branches and of unusually elongating and normal sized fertile-appendages showed that the morphogenetic pattern of synangium development was similar. Anatomical and morphological evidence showed the synangium to be derived from terminal subdivisions or bifurcations of the apical meristem of each structure studied. This supports the phyletic concept that the synangium of the Psilotaceae is basically terminal to an axis or an axis homologue, and that it probably evolved from terminal bifurcative branching. Occasional multiple sporangium lobes may be formed on a P. nudum synangium which may not be represented by vascular bundles. Two hypothetical phyletic models of synangium evolution are proposed that could be used to explain this phenomenon and which should be tested by further evidence. Typical and appendageless P. nudum were compared in their morphogenetic pattern developed at the upper axis vegetative apical meristem, and a reconciliation was made between the structuring of the apparently disparate forms, which involved the presence or absence of serial ordering in apical derivatives. It is suggested that this could serve as a model for appendage evolution in the family Psilotaceae.     

Evolutionary relationships among photosynthetic prokaryotes (Heliobacterium chlorum, Chloroflexus aurantiacus, cyanobacteria, Chlorobium tepidum and proteobacteria): implications regarding the origin of photosynthesis

The presence of shared conserved insertions or deletions in proteins (referred to as signature sequences) provides a powerful means to deduce the evolutionary relationships among prokaryotic organisms. This approach was used in the present work to deduce the branching orders of various eubacterial taxa consisting of photosynthetic organisms. For this purpose, portions of the Hsp60 and Hsp70 genes, covering known signature sequence regions, were PCR-amplified and sequenced from Heliobacterium chlorum, Chloroflexus aurantiacus and Chlorobium tepidum. This information was integrated with sequence data for several other proteins from numerous species to deduce the branching orders of different photosynthetic taxa. Based on signature sequences that are present in different proteins, it is possible to infer that the various eubacterial phyla evolved from a common ancestor in the following order: low G+C Gram-positive (H. chlorum) --> high G+C Gram-positive --> Deinococcus-Thermus --> green non-sulphur bacteria (Cf. aurantiacus ) --> cyanobacteria --> spirochaetes --> Chlamydia-Cytophaga-Aquifex-flavobacteria-green sulphur bacteria (Cb. tepidum) --> proteobacteria (alpha, delta and epsilon) and --> proteobacteria (beta and gamma). The members of the Heliobacteriaceae family that contain a Fe-S type of reaction centre (RC-1) and represent the sole photosynthetic phylum from the Gram-positive or monoderm group of prokaryotes are indicated to be the most ancestral of the photosynthetic lineages. Among the Gram-negative bacteria or diderm prokaryotes, green non-sulphur bacteria such as Cf. aurantiacus, which contains a pheophytin-quinone type of reaction centre (RC-2), are indicated to have evolved very early. Thus, the organisms containing either RC-1 or RC-2 existed before the evolution of cyanobacteria, which contain both these reaction centres to carry out oxygenic photosynthesis. The eubacterial divisions consisting of green sulphur bacteria and proteobacteria are indicated to have diverged after cyanobacteria. Some implications of these results concerning the origin of photosynthesis and the earliest prokaryotic fossils are discussed.     

Arthropod body-plan evolution in the Cambrian with an example from anomalocaridid muscle

The ancestor of the arthropods is widely thought to have possessed a hydrostatic skeleton surrounded by peripheral longitudinal and circular musculature, as exhibited by the extant onychophorans. However, the transition to a lever-style musculature system with an articulating exoskeleton poses a difficult problem in functional evolution: did the musculature or the exoskeleton evolve first, and how? Here, by reference to the musculature of the Lower Cambrian stem-group arthropod Pambdelurion, the problem is resolved in terms of preadaptation and functional degeneracy without recourse to saltational notions. Cambrian taxa lying in the stem-groups of the modern phyla may thus be shown to provide unique evidence for the functional progression involved in the assembly of the extant body plans and obviate the need for exotic genetic or developmental mechanisms to explain the evolution of integrated and complex body plans. The notion of the phylum representing a particularly significant level of organization is thereby brought into question.     

THE EFFECTS OF BODY MASS,PHYLOGENY, HABITAT,AND TROPHIC LEVEL ON MAMMALIAN AGE AT FIRST REPRODUCTION

I examined age at first reproduction of 547 mammalian species to determine the influence of diet and habitat on the evolution of life-history traits. Body mass correlated positively with age at first reproduction, explaining 56% of the variance. Habitat and trophic groups deviated significantly from the allometric curve in a pattern generally consistent with predictions from r/K selection theory and its modifications. However, mammalian orders also deviated significantly from the allometric curve, and different habitat and diet groups contained different ratios of mammalian orders. When the effects of orders were removed, residual deviations did not differ among ecological groups. Adjusting for ecological differences did not eliminate the differences between orders. These results suggest that body mass (or some correlated factor) and phylogeny strongly constrain age at first reproduction. Ecological factors appear to have little effect on the evolution of age at first reproduction. Apparent differences in weight-specific ages at first reproduction within habitats and trophic groups may be the result of ecological selection of order composition in the present, rather than ecologically driven evolution of life history in the past.     

Ontogeny and phyletic size change in living and fossil lemurs

Lemurs are notable for encompassing the range of body‐size variation for all primates past and present—close to four orders of magnitude. Benefiting from the phylogenetic proximity of subfossil lemurs to smaller‐bodied living forms, we employ allometric data from the skull to probe the ontogenetic bases of size differentiation and morphological diversity across these clades. Building upon prior pairwise comparisons between sister taxa, we performed the first clade‐wide analyses of craniomandibular growth allometries in 359 specimens from 10 lemuroids and 176 specimens from 8 indrioids. Ontogenetic trajectories for extant forms were used as a criterion of subtraction to evaluate morphological variation, and putative adaptations among sister taxa. In other words, do species‐level differences in skull form result from the differential extension of common patterns of relative growth? In lemuroids, a pervasive pattern of ontogenetic scaling is observed for facial dimensions in all genera, with three genera also sharing relative growth trajectories for jaw proportions (Lemur, Eulemur, Varecia). Differences in masticatory growth and form characterizing Hapalemur and fossil Pachylemur likely reflect dietary factors. Pervasive ontogenetic scaling characterizes the facial skull in extant Indri, Avahi, and Propithecus, as well as their larger, extinct sister taxa Mesopropithecus and Babakotia. Significant interspecific differences are observed in the allometry of indrioid masticatory proportions, with variation in the mechanical advantage of the jaw adductors and stress‐resisting elements correlated with diet. As the growth series and adult data are largely coincidental in each clade, interspecific variation in facial form may result from selection for body‐size differentiation among sister taxa. Those cases where trajectories are discordant identify potential dietary adaptations linked to variation in masticatory forces during chewing and biting. Although such dissociations highlight selection to uncouple shared ancestral growth patterns, they occur largely via transpositions and retention of primitive size‐shape covariation patterns or relative growth coefficients. Am. J. Primatol. 72:161–172, 2010. © 2009 Wiley‐Liss, Inc.     

SIZE VARIATION,GROWTH STRATEGIES,AND THE EVOLUTION OF MODULARITY IN THE MAMMALIAN SKULL

Allometry is a major determinant of within‐population patterns of association among traits and, therefore, a major component of morphological integration studies. Even so, the influence of size variation over evolutionary change has been largely unappreciated. Here, we explore the interplay between allometric size variation, modularity, and life‐history strategies in the skull from representatives of 35 mammalian families. We start by removing size variation from within‐species data and analyzing its influence on integration magnitudes, modularity patterns, and responses to selection. We also carry out a simulation in which we artificially alter the influence of size variation in within‐taxa matrices. Finally, we explore the relationship between size variation and different growth strategies. We demonstrate that a large portion of the evolution of modularity in the mammalian skull is associated to the evolution of growth strategies. Lineages with highly altricial neonates have adult variation patterns dominated by size variation, leading to high correlations among traits regardless of any underlying modular process and impacting directly their potential to respond to selection. Greater influence of size variation is associated to larger intermodule correlations, less individualized modules, and less flexible responses to natural selection.     

Haeckel's ABC of evolution and development

One of the central, unresolved controversies in biology concerns the distribution of primitive versus advanced characters at different stages of vertebrate development. This controversy has major implications for evolutionary developmental biology and phylogenetics. Ernst Haeckel addressed the issue with his Biogenetic Law, and his embryo drawings functioned as supporting data. We re-examine Haeckel's work and its significance for modern efforts to develop a rigorous comparative framework for developmental studies. Haeckel's comparative embryology was evolutionary but non-quantitative. It was based on developmental sequences, and treated heterochrony as a sequence change. It is not always clear whether he believed in recapitulation of single characters or entire stages. The Biogenetic Law is supported by several recent studies -- if applied to single characters only. Haeckel's important but overlooked alphabetical analogy of evolution and development is an advance on von Baer. Haeckel recognized the evolutionary diversity in early embryonic stages, in line with modern thinking. He did not necessarily advocate the strict form of recapitulation and terminal addition commonly attributed to him. Haeckel's much-criticized embryo drawings are important as phylogenetic hypotheses, teaching aids, and evidence for evolution. While some criticisms of the drawings are legitimate, others are more tendentious. In opposition to Haeckel and his embryo drawings, Wilhelm His made major advances towards developing a quantitative comparative embryology based on morphometrics. Unfortunately His's work in this area is largely forgotten. Despite his obvious flaws, Haeckel can be seen as the father of a sequence-based phylogenetic embryology.     

Active and resting metabolism in birds: allometry, phylogeny and ecology

Variation in resting metabolic rate is strongly correlated with differences in body weight among birds. The lowest taxonomic level at which most of the variance in resting metabolic rate and body weight is evident for the sample is among families within orders. The allometric exponent across family points is 0.67. This exponent accords with the surface area interpretation of metabolic scaling based on considerations of heat loss. Deviations of family points from this allometric line are used to examine how resting metabolic rates differ among taxa, and whether variation in resting metabolic rate is correlated with broad differences in ecology and behaviour. Despite the strong correlation between resting metabolic rate and body weight, there is evidence for adaptive departures from the allometric line, and possible selective forces are discussed.
The allometric scaling of active metabolic rate is compared with that of resting metabolic rate. The allometric exponents for the two levels of energy expenditure differ, demonstrating that active small-bodied birds require proportionately more energy per unit time above resting levels than do active large-bodied birds. No consistent evidence was found to indicate that the different methods used to estimate active metabolic rate result in systematic bias. Birds require more energy relative to body size when undertaking breeding activities than at other stages of the annual cycle.     

The allometric approach to species differences in brain size

Allometric methods can be used to test quantitative theories of the relationship between brain size and body size across species, and to search for ecological, behavioural, life history, and ontogenetic correlates of brain size. Brain size scales with an allometric exponent of around 0.75 against body size across mammals, but is closer to 0.56 for birds and for reptiles. The slope of the allometric line often varies depending upon the taxonomic level of analysis. However, this phenomenon, at least in mammals, may be a statistical artifact. Brain size for a given body size (relative brain size) varies among orders in birds and mammals, and some dietary associations with relative brain size have been found in particular taxa. Developmental status at birth is the most consistent correlate of relative brain size: precocial neonates have larger brains for a given maternal size than altricial neonates in both birds and mammals. Altricial neonates, however, have more brain growth following birth, and in birds also have larger relative adult brain sizes. Energetic explanations for differences in neonatal brain growth, although attractive on theoretical grounds, have largely failed to stand up to empirical tests.     

Evolutionary analyses of genes in Echinodermata offer insights towards the origin of metazoan phyla

Despite recent studies discussing the evolutionary impacts of gene duplications and losses among metazoans, the genomic basis for the evolution of phyla remains enigmatic. Here, we employ phylogenomic approaches to search for orthologous genes without known functions among echinoderms, and subsequently use them to guide the identification of their homologs across other metazoans. Our final set of 14 genes was obtained via a suite of homology prediction tools, gene expression data, gene ontology, and generating the Strongylocentrotus purpuratus phylome. The gene set was subjected to selection pressure analyses, which indicated that they are highly conserved and under negative selection. Their presence across broad taxonomic depths suggests that genes required to form a phylum are ancestral to that phylum. Therefore, rather than de novo gene genesis, we posit that evolutionary forces such as selection on existing genomic elements over large timescales may drive divergence and contribute to the emergence of phyla.     

Allometry of egg and hatchling mass in birds and reptiles: roles of developmental maturity, eggshell structure and phylogeny

The factors determining hatchling mass (HM) are investigated in a wide range of birds and reptiles using regression analysis, analysis of covariance and comparative analysis by independent contrasts. In birds, initial egg mass (IEM) at laying is the most important factor affecting HM and phylogenetic relatedness has no significant effects on HM. Developmental maturity of the avian neonates did not affect the proportion of IEM converted into HM. For all reptile species, IEM also significantly affected HM but phylogenetic relatedness did not. By contrast, allometric relationships between IEM and HM in the different orders of reptiles were affected by shell type. The robustness of allometric relationships across taxa in birds and reptiles suggests that there is a physiological link between IEM and HM, which contrasts with that observed for the relationship between egg mass and incubation period. This result has significant implications for the inter-relationships between IEM and embryonic growth, which are discussed for birds and reptiles.     

Body mass and temperature influence rates of mitochondrial DNA evolution in North American cyprinid fish

The mass-specific metabolic rate hypothesis of Gillooly and others predicts that DNA mutation and substitution rates are a function of body mass and temperature. We tested this hypothesis with sequence divergences estimated from mtDNA cytochrome b sequences of 54 taxa of cyprinid fish. Branch lengths estimated from a likelihood tree were compared with metabolic rates calculated from body mass and environmental temperatures experienced by those taxa. The problem of unknown age estimates of lineage splitting was avoided by comparing estimated amounts of metabolic activity along phyletic lines leading to pairs of modern taxa from their most recent common ancestor with sequence divergences along those same pairs of phyletic lines. There were significantly more pairs for which the phyletic line with greater genetic change also had the higher metabolic activity, when compared to the prediction of a hypothesis that body mass and temperature are not related to substitution rate.