Daniel W. McShea

MECHANISMS OF LARGE-SCALE EVOLUTIONARY TRENDS

Large‐scale evolutionary trends may result from driving forces or from passive diffusion in bounded spaces. Such trends are persistent directional changes in higher taxa spanning significant periods of geological time; examples include the frequently cited long‐term trends in size, complexity, and fitness in life as a whole, as well as trends in lesser supraspecific taxa and trends in space. In a driven trend, the distribution mean increases on account of a force (which may manifest itself as a bias in the direction of change) that acts on lineages throughout the space in which diversification occurs. In a passive system, no pervasive force or bias exists, but the mean increases because change in one direction is blocked by a boundary, or other inhomogeneity, in some limited region of the space. Two tests have been used to distinguish these trend mechanisms: (1) the test based on the behavior of the minimum; and (2) the ancestor‐descendant test, based on comparisons in a random sample of ancestor‐descendant pairs that lie far from any possible lower bound. For skewed distributions, a third test is introduced here: (3) the subclade test, based on the mean skewness of a sample of subclades drawn from the tail of a terminal distribution. With certain restrictions, a system is driven if the minimum increases, if increases significantly outnumber decreases among ancestor‐descendant pairs, and if the mean skew of subclades is significantly positive. A passive mechanism is more difficult to demonstrate but is the more likely mechanism if decreases outnumber increases and if the mean skew of subclades is negative. Unlike the other tests, the subclade test requires no detailed phylogeny or paleontological time series, but only terminal (e.g., modern) distributions. Monte Carlo simulations of the diversification of a clade are used to show how the subclade test works. In the empirical cases examined, the three tests gave concordant results, suggesting first, that they work, and second, that the passive and driven mechanisms may correspond to natural categories of causes of large‐scale trends.

Individual versus social complexity, with particular reference to ant colonies.

Insect societies – colonies of ants, bees, wasps and termites – vary enormously in their social complexity. Social complexity is a broadly used term that encompasses many individual and colony‐level traits and characteristics such as colony size, polymorphism and foraging strategy. A number of earlier studies have considered the relationships among various correlates of social complexity in insect societies; in this review, we build upon those studies by proposing additional correlates and show how all correlates can be integrated in a common explanatory framework. The various correlates are divided among four broad categories (sections). Under ‘polyphenism’ we consider the differences among individuals, in particular focusing upon ‘caste’ and specialization of individuals. This is followed by a section on ‘totipotency’ in which we consider the autonomy and subjugation of individuals. Under this heading we consider various aspects such as intracolony conflict, worker reproductive potential and physiological or morphological restrictions which limit individuals’ capacities to perform a range of tasks or functions. A section entitled ‘organization of work’ considers a variety of aspects, e.g. the ability to tackle group, team or partitioned tasks, foraging strategies and colony reliability and efficiency. A final section,‘communication and functional integration’, considers how individual activity is coordinated to produce an integrated and adaptive colony. Within each section we use illustrative examples drawn from the social insect literature (mostly from ants, for which there is the best data) to illustrate concepts or trends and make a number of predictions concerning how a particular trait is expected to correlate with other aspects of social complexity. Within each section we also expand the scope of the arguments to consider these relationships in a much broader sense ofsociality’ by drawing parallels with other ‘social’ entities such as multicellular individuals, which can be understood as ‘societies’ of cells. The aim is to draw out any parallels and common causal relationships among the correlates. Two themes run through the study. The first is the role of colony size as an important factor affecting social complexity. The second is the complexity of individual workers in relation to the complexity of the colony. Consequently, this is an ideal opportunity to test a previously proposed hypothesis that ‘individuals of highly social ant species are less complex than individuals from simple ant species’ in light of numerous social correlates. Our findings support this hypothesis. In summary, we conclude that, in general, complex societies are characterized by large colony size, worker polymorphism, strong behavioural specialization and loss of totipotency in its workers, low individual complexity, decentralized colony control and high system redundancy, low individual competence, a high degree of worker cooperation when tackling tasks, group foraging strategies, high tempo, multi‐chambered tailor‐made nests, high functional integration, relatively greater use of cues and modulatory signals to coordinate individuals and heterogeneous patterns of worker‐worker interaction. Key words: Ants, insect societies, individual complexity, social complexity, polyphenism, totitpotency, work organization, functional integration, sociality.

Complexity and Evolution: What Everybody Knows

The consensus among evolutionists seems to be (and has been for at least a century) that the morphological complexity of organisms increases in evolution, although almost no empirical evidence for such a trend exists. Most studies of complexity have been theoretical, and the few empirical studies have not, with the exception of certain recent ones, been especially rigorous; reviews are presented of both the theoretical and empirical literature. The paucity of evidence raises the question of what sustains the consensus, and a number of suggestions are offered, including the possibility that certain cultural and/or perceptual biases are at work. In addition, a shift in emphasis from theoretical to empirical inquiry is recommended for the study of complexity, and guidelines for future empirical studies are proposed.

Detecting changes in morphospace occupation patterns in the fossil record: characterization and analysis of measures of disparity

Abstract Recently, there has been much interest in detecting and measuring patterns of change in disparity. Although most studies have used one or two measures of disparity to quantify and characterize the occupation of morphospace, multiple measures may be necessary to fully detect changes in patterns of morphospace occupation. Also, the ability to detect morphological trends and occupation patterns within morphospace depends on using the appropriate measure(s) of disparity. In this study, seven measures were used to determine and characterize sensitivity to sample size of the data, number of morphological characters, percentage of missing data, and changes in morphospace occupation pattern. These consist of five distance measures—sum of univariate variances, total range, mean distance, principal coordinate analysis volume, average pairwise dissimilarity—and two non-distance measures—participation ratio and number of unique pairwise character combinations. Evaluation of each measure with respect to sensitivity to sample size, number of morphological characters, and percentage of missing data was accomplished by using both simulated and Ordovician crinoid data. For simulated data, each measure of disparity was evaluated for its response to changes of morphospace occupation pattern, and with respect to simulated random and nonrandom extinction events. Changes in disparity were also measured within the Crinoidea across the Permian extinction event. Although all measures vary in sensitivity with respect to species sample size, number of morphological characters, and percentage of missing data, the non-distance measures overall produce the lowest estimates of variance (in bootstrap analyses). The non-distance measures appear to be relatively insensitive to changes in morphospace occupation pattern. All measures, except average pairwise dissimilarity, detect changes in occupation pattern in simulated nonrandom extinction events, but all measures, except number of unique pairwise character combinations and principal coordinate analysis volume, are relatively insensitive to changes in pattern in simulated random extinction events. The distance measures report similar changes in disparity over the Permian extinction event, whereas the non-distance measures differ. This study suggests that each measure of disparity is designed for different purposes, and that by using a combination of techniques a clearer picture of disparity should emerge.

PERSPECTIVE METAZOAN COMPLEXITY AND EVOLUTION: IS THERE A TREND?

The notion that complexity increases in evolution is widely accepted, but the best‐known evidence is highly impressionistic. Here I propose a scheme for understanding complexity that provides a conceptual basis for objective measurement. The scheme also shows complexity to be a broad term covering four independent types. For each type, I describe some of the measures that have been devised and review the evidence for trends in the maximum and mean. In metazoans as a whole, there is good evidence only for an early‐Phanerozoic trend, and only in one type of complexity. For each of the other types, some trends have been documented, but only in a small number of metazoan subgroups.

Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity

The maximum size of organisms has increased enormously since the initial appearance of life >3.5 billion years ago (Gya), but the pattern and timing of this size increase is poorly known. Consequently, controls underlying the size spectrum of the global biota have been difficult to evaluate. Our period-level compilation of the largest known fossil organisms demonstrates that maximum size increased by 16 orders of magnitude since life first appeared in the fossil record. The great majority of the increase is accounted for by 2 discrete steps of approximately equal magnitude: the first in the middle of the Paleoproterozoic Era (≈1.9 Gya) and the second during the late Neoproterozoic and early Paleozoic eras (0.6–0.45 Gya). Each size step required a major innovation in organismal complexity—first the eukaryotic cell and later eukaryotic multicellularity. These size steps coincide with, or slightly postdate, increases in the concentration of atmospheric oxygen, suggesting latent evolutionary potential was realized soon after environmental limitations were removed.

Functional Complexity in Organisms: Parts as Proxies

The functional complexity, or the number of functions, of organisms hasfigured prominently in certain theoretical and empirical work inevolutionary biology. Large-scale trends in functional complexity andcorrelations between functional complexity and other variables, such assize, have been proposed. However, the notion of number of functions hasalso been operationally intractable, in that no method has been developedfor counting functions in an organism in a systematic and reliable way.Thus, studies have had to rely on the largely unsupported assumption thatnumber of functions can be measured indirectly, by using number ofmorphological, physiological, and behavioral “parts” as a proxy. Here, amodel is developed that supports this assumption. Specifically, the modelpredicts that few parts will have many functions overlapping in them, andtherefore the variance in number of functions per part will be low. If so,then number of parts is expected to be well correlated with number offunctions, and we can use part counts as proxies for function counts incomparative studies of organisms, even when part counts are low. Alsodiscussed briefly is a strategy for identifying certain kinds of parts inorganisms in a systematic way.

The hierarchical structure of organisms: a scale and documentation of a trend in the maximum

Abstract The degree of hierarchical structure of organisms—the number of levels of nesting of lower-level entities within higher-level individuals—has apparently increased a number of times in the history of life, notably in the origin of the eukaryotic cell from an association of prokaryotic cells, of multicellular organisms from clones of eukaryotic cells, and of integrated colonies from aggregates of multicellular individuals. Arranged in order of first occurrence, these three transitions suggest a trend, in particular a trend in the maximum, or an increase in the degree of hierarchical structure present in the hierarchically deepest organism on Earth. However, no rigorous documentation of such a trend—based on operational and consistent criteria for hierarchical levels—has been attempted. Also, the trajectory of increase has not been examined in any detail. One limitation is that no hierarchy scale has been developed with sufficient resolution to document more than these three major increases. Here, a higher-resolution scale is proposed in which hierarchical structure is decomposed into levels and sublevels, with levels reflecting number of layers of nestedness, and sublevels reflecting degree of individuation at the highest level. The scale is then used, together with the body-fossil record, to plot the trajectory of the maximum. Two alternative interpretations of the record are considered, and both reveal a long-term trend extending from the Archean through the early Phanerozoic. In one, the pattern of increase was incremental, with almost all sublevels arising precisely in order. The data also raise the possibility that waiting times for transitions between sublevels may have decreased with increasing hierarchical level (and with time). These last two findings—incremental increase in level and decreasing waiting times—are tentative, pending a study of possible biases in the fossil record.

Evolutionary change in the morphological complexity of the mammalian vertebral column

The notion that morphological complexity increases in evolution is widely accepted in biology and paleontology. Several possible explanations have been offered for this trend, among them the suggestion that it has an active forcing mechanism, such as natural selection or the second law of thermodynamics. No such mechanism has yet been empirically demonstrated, but testing is possible: if a forcing mechanism has operated, the expectation is that complexity would have increased in evolutionary lineages more frequently than it decreased. However, a quantitative analysis of changes in the complexity of the vertebral column in a random sample of mammalian lineages reveals a nearly equal number of increases and decreases. This finding raises the possibility that no forcing mechanism exists, or at least that it may not be as powerful or pervasive as has been assumed. The finding also highlights the need for more empirical tests.

The evolution of complexity without natural selection, a possible large-scale trend of the fourth kind

Abstract A simple principle predicts a tendency, or vector, toward increasing organismal complexity in the history of life: As the parts of an organism accumulate variations in evolution, they should tend to become more different from each other. In other words, the variance among the parts, or what I call the “internal variance” of the organism, will tend to increase spontaneously. Internal variance is complexity, I argue, albeit complexity in a purely structural sense, divorced from any notion of function. If the principle is correct, this tendency should exist in all lineages, and the resulting trend (if there is one) will be driven, or more precisely, driven by constraint (as opposed to selection). The existence of a trend is uncertain, because the internal-variance principle predicts only that the range of options offered up to selection will be increasingly complex, on average. And it is unclear whether selection will enhance this vector, act neutrally, or oppose it, perhaps negating it. The vector might also be negated if variations producing certain kinds of developmental truncations are especially common in evolution. Constraint-driven trends—or what I call large-scale trends of the fourth kind—have been in bad odor in evolutionary studies since the Modern Synthesis. Indeed, one such trend, orthogenesis, is famous for having been discredited. In Stephen Jay Goulds last book, The Structure of Evolutionary Thought, he tried to rehabilitate this category (although not orthogenesis), showing how constraint-driven trends could be produced by processes well within the mainstream of contemporary evolutionary theory. The internal-variance principle contributes to Goulds project by adding another candidate trend to this category.