Evolutionary trends and goal directedness.

The conventional wisdom declares that evolution is not goal directed, that teleological considerations play no part in our understanding of evolutionary trends. Here I argue that, to the contrary, under a current view of teleology, field theory, most evolutionary trends would have to be considered goal directed to some degree. Further, this view is consistent with a modern scientific outlook, and more particularly with evolutionary theory today. Field theory argues that goal directedness is produced by higher-level fields that direct entities contained within them to behave persistently and plastically, that is, returning them to a goal-directed trajectory following perturbations (persistence) and directing them to a goal-directed trajectory from a large range of alternative starting points (plasticity). The behavior of a bacterium climbing a chemical food gradient is persistent and plastic, with guidance provided by the external "food field," the chemical gradient. Likewise, an evolutionary trend that is produced by natural selection is a lineage behaving persistently and plastically under the direction of its local ecology, an "ecological field." Trends directed by selection-generated boundaries, thermodynamic gradients, and certain internal constraints, would also count as goal directed. In other words, most of the causes of evolutionary trends that have been proposed imply goal directedness. However, under field theory, not all trends are goal directed. Examples are discussed. Importantly, nothing in this view suggests that evolution is guided by intentionality, at least none at the level of animal intentionality. Finally, possible implications for our thinking about evolutionary directionality in the history of life are discussed.

Four reasons for scepticism about a human major transition in social individuality.

The 'major transitions in evolution' are mainly about the rise of hierarchy, new individuals arising at ever higher levels of nestedness, in particular the eukaryotic cell arising from prokaryotes, multicellular individuals from solitary protists and individuated societies from multicellular individuals. Some lists include human societies as a major transition, but based on a comparison with the non-human transitions, there are reasons for scepticism. (i) The foundation of the major transitions is hierarchy, but the cross-cutting interactions in human societies undermine hierarchical structure. (ii) Natural selection operates in three modes-stability, growth and reproductive success-and only the third produces the complex adaptations seen in fully individuated higher levels. But human societies probably evolve mainly in the stability and growth modes. (iii) Highly individuated entities are marked by division of labour and commitment to morphological differentiation, but in humans differentiation is mostly behavioural and mostly reversible. (iv) As higher-level individuals arise, selection drains complexity, drains parts, from lower-level individuals. But there is little evidence of a drain in humans. In sum, a comparison with the other transitions gives reasons to doubt that human social individuation has proceeded very far, or if it has, to doubt that it is a transition of the same sort. This article is part of the theme issue 'Human socio-cultural evolution in light of evolutionary transitions'.

A quantitative formulation of biology's first law.

The zero-force evolutionary law (ZFEL) states that in evolutionary systems, in the absence of forces or constraints, diversity and complexity tend to increase. The reason is that diversity and complexity are both variance measures, and variances tend to increase spontaneously as random events accumulate. Here, we use random-walk models to quantify the ZFEL expectation, producing equations that give the probabilities of diversity or complexity increasing as a function of time, and that give the expected magnitude of the increase. We produce two sets of equations, one for the case in which variation occurs in discrete steps, the other for the case in which variation is continuous. The equations provide a way to decompose actual trajectories of diversity or complexity into two components, the portion due to the ZFEL and a remainder due to selection and constraint. Application of the equations is demonstrated using real and hypothetical data.

Hierarchical complexity and the size limits of life.

Over the past 3.8 billion years, the maximum size of life has increased by approximately 18 orders of magnitude. Much of this increase is associated with two major evolutionary innovations: the evolution of eukaryotes from prokaryotic cells approximately 1.9 billion years ago (Ga), and multicellular life diversifying from unicellular ancestors approximately 0.6 Ga. However, the quantitative relationship between organismal size and structural complexity remains poorly documented. We assessed this relationship using a comprehensive dataset that includes organismal size and level of biological complexity for 11 172 extant genera. We find that the distributions of sizes within complexity levels are unimodal, whereas the aggregate distribution is multimodal. Moreover, both the mean size and the range of size occupied increases with each additional level of complexity. Increases in size range are non-symmetric: the maximum organismal size increases more than the minimum. The majority of the observed increase in organismal size over the history of life on the Earth is accounted for by two discrete jumps in complexity rather than evolutionary trends within levels of complexity. Our results provide quantitative support for an evolutionary expansion away from a minimal size constraint and suggest a fundamental rescaling of the constraints on minimal and maximal size as biological complexity increases.

Logic, passion and the problem of convergence.

Our estimate of the likelihood of convergence on human-style intelligence depends on how we understand our various mental capacities. Here I revive David Hume's theory of motivation and action to argue that the most common understanding of the two conventionally recognized components of intelligence-reason and emotion-is confused. We say things like, 'Reason can overcome emotion', but to make this statement meaningful, we are forced to treat reason as a compound notion, as a forced and unhappy mixture of concepts that are incommensurate. An alternative is to parse intelligence in a different way, into two sets of capacities: (i) non-affective capacities, including logic, calculation and problem-solving; (ii) affective capacities, including wants, preferences and cares, along with the emotions. Thus, the question of convergence becomes two questions, one having to do with affective and one with non-affective capacities. What is the likelihood of convergence of these in non-human lineages, in other ecologies, on other worlds? Given certain assumptions, convergence of the non-affective capacities in thinking species seems likely, I argue, while convergence of the affective capacities seems much less likely.

Freedom and purpose in biology.

All seemingly teleological systems share a common hierarchical structure. They consist of a small entity moving or changing within a larger field that directs it from above (what I call "upper direction"). This is true for organisms seeking some external resource, for the organized behavior of cells and other parts in organismal development, and for lineages evolving by natural selection. In all cases, the lower-level entity is partly "free," tending to wander under the influence of purely local forces, and partly directed by a larger enveloping field. The persistent and plastic behavior that characterizes goal-directedness arises, I argue, at intermediate levels of freedom and upper direction, when the two are in a delicate balance. I tentatively extend the argument to human teleology (wants, purposes).

Machine wanting.

Wants, preferences, and cares are physical things or events, not ideas or propositions, and therefore no chain of pure logic can conclude with a want, preference, or care. It follows that no pure-logic machine will ever want, prefer, or care. And its behavior will never be driven in the way that deliberate human behavior is driven, in other words, it will not be motivated or goal directed. Therefore, if we want to simulate human-style interactions with the world, we will need to first understand the physical structure of goal-directed systems. I argue that all such systems share a common nested structure, consisting of a smaller entity that moves within and is driven by a larger field that contains it. In such systems, the smaller contained entity is directed by the field, but also moves to some degree independently of it, allowing the entity to deviate and return, to show the plasticity and persistence that is characteristic of goal direction. If all this is right, then human want-driven behavior probably involves a behavior-generating mechanism that is contained within a neural field of some kind. In principle, for goal directedness generally, the containment can be virtual, raising the possibility that want-driven behavior could be simulated in standard computational systems. But there are also reasons to believe that goal-direction works better when containment is also physical, suggesting that a new kind of hardware may be necessary.

Drosophila mutants suggest a strong drive toward complexity in evolution.

The view that complexity increases in evolution is uncontroversial, yet little is known about the possible causes of such a trend. One hypothesis, the Zero Force Evolutionary Law (ZFEL), predicts a strong drive toward complexity, although such a tendency can be overwhelmed by selection and constraints. In the absence of strong opposition, heritable variation accumulates and complexity increases. In order to investigate this claim, we evaluate the gross morphological complexity of laboratory mutants in Drosophila melanogaster, which represent organisms that arise in a context where selective forces are greatly reduced. Complexity was measured with respect to part types, shape, and color over two independent focal levels. Compared to the wild type, we find that D. melanogaster mutants are significantly more complex. When the parts of mutants are categorized by degree of constraint, we find that weakly constrained parts are significantly more complex than more constrained parts. These results support the ZFEL hypothesis. They also represent a first step in establishing the domain of application of the ZFEL and show one way in which a larger empirical investigation of the principle might proceed.

The evolutionary consequences of oxygenic photosynthesis: a body size perspective.

The high concentration of molecular oxygen in Earth's atmosphere is arguably the most conspicuous and geologically important signature of life. Earth's early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0-2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O(2):CO(2). Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio-rather than mass or volume-predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.

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 (approximately 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.

Origin and evolution of large brains in toothed whales.

Toothed whales (order Cetacea: suborder Odontoceti) are highly encephalized, possessing brains that are significantly larger than expected for their body sizes. In particular, the odontocete superfamily Delphinoidea (dolphins, porpoises, belugas, and narwhals) comprises numerous species with encephalization levels second only to modern humans and greater than all other mammals. Odontocetes have also demonstrated behavioral faculties previously only ascribed to humans and, to some extent, other great apes. How did the large brains of odontocetes evolve? To begin to investigate this question, we quantified and averaged estimates of brain and body size for 36 fossil cetacean species using computed tomography and analyzed these data along with those for modern odontocetes. We provide the first description and statistical tests of the pattern of change in brain size relative to body size in cetaceans over 47 million years. We show that brain size increased significantly in two critical phases in the evolution of odontocetes. The first increase occurred with the origin of odontocetes from the ancestral group Archaeoceti near the Eocene-Oligocene boundary and was accompanied by a decrease in body size. The second occurred in the origin of Delphinoidea only by 15 million years ago.

Three puzzles in hierarchical evolution.

The maximum degree of hierarchical structure of organisms has risen over the history of life, notably in three transitions: the origin of the eukaryotic cell from symbiotic associations of prokaryotes; the emergence of the first multicellular individuals from clones of eukaryotic cells; and the origin of the first individuated colonies from associations of multicellular organisms. The trend is obvious in the fossil record, but documenting it using a high-resolution hierarchy scale reveals three puzzles: 1) the rate of origin of new levels accelerates, at least until the early Phanerozoic; 2) after that, the trend may slow or even stop; and 3) levels may sometimes arise out of order. The three puzzles and their implications are discussed; a possible explanation is offered for the first.

A complexity drain on cells in the evolution of multicellularity.

A hypothesis has been advanced recently predicting that, in evolution, as higher-level entities arise from associations of lower-level organisms, and as these entities acquire the ability to feed, reproduce, defend themselves, and so on, the lower-level organisms will tend to lose much of their internal complexity (McShea 2001a). In other words, in hierarchical transitions, there is a drain on numbers of part types at the lower level. One possible rationale is that the transfer of functional demands to the higher level renders many part types at the lower level useless, and thus their loss in evolution is favored by selection for economy. Here, a test is conducted at the cell level, comparing numbers of part types in free-living eukaryotic cells (protists) and the cells of metazoans and land plants. Differences are significant and consistent with the hypothesis, suggesting that tests at other hierarchical levels may be worthwhile.

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.

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.

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.