Function Over Form:
Phenotypic Integration and the Evolution of the Mammalian Skull

By Claire Asher, on 8 December 2014

Our bodies are more than just a collection of independent parts – they are complex, integrated systems that rely upon precise coordination in order to function properly. In order for a leg to function as a leg, the bones, muscles, ligaments, nerves and blood vessels must all work together as an integrated whole. This concept, known as phenotypic integration, is a pervasive characteristic of living organisms, and recent research in GEE suggests that it may have a profound influence on the direction and magnitude of evolutionary change.

Phenotypic integration explains how multiple traits, encoded by hundreds of different genes, can evolve and develop together such that the functional unit (a leg, an eye, the circulatory system) fulfils its desired role. Phenotypic integration could be complete – every trait is interrelated and could show correlated evolution. However, theoretical and empirical data suggest that it is more commonly modular, with strong phenotypic integration within functional modules. This modularity represents a compromise between a total lack of trait coordination (which would allow evolution to breakdown functional phenotypic units) and the evolutionary inflexibility of complete integration. Understanding phenotypic integration and its consequences is therefore important if we are to understand how complex phenotypes respond to natural selection.

Functional modules in mammals, Goswami et al (2014)

Functional modules in mammals, Goswami et al (2014)

It is thought that phenotypic integration is likely to constrain evolution and render certain phenotypes impossible if their evolution would require even temporary disintegration of a functional module. However, integration may also facilitate evolution by coordinating the responses of traits within a functional unit. Recent research by GEE academic Dr Anjali Goswami and colleagues sought to understand the evolutionary implications of phenotypic integration in mammals.

Expanding on existing mathematical models, and applying these to data from 1635 skulls from nearly 100 different mammal species including placental mammals, marsupials and monotremes, Dr Goswami investigated the effect of phenotypic integration on evolvability and respondability to natural selection. Comparing between a model with two functional modules in the mammalian skull and a model with six, the authors found greater support for a larger number of functional modules. Monotremes, whose skulls may be subject to different selection pressures due to their unusual life history, did not fit this pattern and may have undergone changes in cranial modularity during the early evolution of mammals. Compared with random simulations, real mammal skulls tend to be either more or less disparate from each other, suggesting that phenotypic integration may both constrain and facilitate evolution under different circumstances. The authors report a strong influence of phenotypic integration on both the magnitude and trajectory of evolutionary responses to selection, although they found no evidence that it influences the speed of evolution.

Thus, phenotypic integration between functional modules appears to have a profound impact on the direction and extent of evolutionary change, and may tend to favour convergent evolution of modules that perform the same function (e.g bird and bat wings for powered flight), by forcing individuals down certain evolutionary trajectories. The influence of phenotypic integration on the speed, direction and magnitude of evolution has important implications for the study of evolution, particularly when analysing fossil remains, since it can make estimates of the timing of evolutionary events more difficult. Failing to incorporate functional modules into models of evolution will likely reduce their accuracy and could produce erroneous results.

Phenotypic integration is what holds together functional units within an organism as a whole, in the face of natural selection. Modularity enables traits to evolve independently when their functions are not strongly interdependent, and prevents evolution from disintegrating functional units. Through these actions, phenotypic integration can constrain or direct evolution in ways that might not be predicted based on analyses of traits individually. This can have important impacts upon the speed, magnitude and direction of evolution, and may tend to favour convergence.

Original Article:

() Global Environmental Change


This research was made possible by support from the Natural Environment Research Council (NERC), and the National Science Foundation (NSF).

Skulls and Teeth: Constraints on Mammalian Evolution

By Claire Asher, on 7 June 2013

When we think about evolution, we tend to imagine the appearance and behaviour of animals as infinitely malleable, changing and adapting to perfectly suit the whim of natural selection. However, in many cases, evolution is actually surprisingly constrained. The potential for a species to evolve into new environments, diets or lifestyles may be limited if the necessary variation isn’t available in the population. In this case, the raw materials for natural selection to act upon are missing and a species cannot evolve in a particular direction. Evolutionary constraints may be developmental or genetic in origin, and may in part explain why some groups of species are more diverse than others.

Early in mammalian evolution, around 160 million years ago, mammals diverged into two main groups; placental mammals (e.g. humans, rats, elephants) and marsupials (e.g. kangaroos, possums, koalas). Placental and marsupial mammals use a different strategy for early development; mammalian infants develop either internally (placental mammals) or in a pouch (marsupials). Despite a similar period of evolutionary history, there are far fewer species of marsupials, and as a group they show less diversity in terms of locomotion and diet. New research suggests their unusual developmental strategy may have constrained their evolution, limiting the variety of present-day marsupials.

A Koala (Phascolarctos cinereus)
A Marsupial Mammal


A Chipmunk (Neotamias umbrinus)
A Placental Mammal

Pouch-Living Limits Marsupial Diversity
Placental mammals give birth to reasonably well-developed young after a lengthy pregnancy. However, marsupials, such as kangaroos and koalas, do things a bit differently. The infant is ejected very early in development, and must crawl to a specialised pouch where it can complete the rest of its development, feeding by suckling. This developmental strategy is pretty demanding on the young marsupial, and requires that they are strong enough to crawl and suckle at a very young age. There is evidence that the shoulder has been constrained by the demands of crawling at a young age. Has suckling imposed similar constraints on the skull?

During development, embryonic connective tissue begins to form into bone through a process known as ossification. In marsupials, ossification in the skull and particularly in facial bones occurs much earlier in development compared to placental mammals. This pattern is probably necessary to allow marsupial young to suckle at such a young age. Early facial ossification has wide-ranging effects on brain, tooth and muscle development, and may have limited the diversity of facial shapes available to marsupials. Suckling may have been a major constraint on marsupial evolution.

Facial bones (viscerocranium)
and braincase (neurocranium)

In a recent study conducted in GEE, Bennett and Goswami (2013) measured a number of skull characteristics for 125 species of placental and marsupial mammals. Previous studies have failed to find evidence for evolutionary constraints affecting mammalian skulls, but these studies primarily focused on carnivores, and considered the whole skull at once. By looking at different regions of the skull separately, Bennett and Goswami found that marsupials exhibit less variation between species in the facial bones (viscerocranium) than placental mammals. This pattern is not present for the braincase (neurocranium), which is not involved in suckling behaviour, and where bones ossify much later. These results suggest that early suckling might have constrained the diversity of marsupial skull shapes, and may go some way to explaining why marsupials are less diverse.

Something to Get Your Teeth Into
Mammalian diversity has probably been constrained by a variety of factors, not just bone ossification. Another recent study from GEE and Earth Sciences by Halliday and Goswami (2013) showed that tooth growth patterns may have restricted the relative size and shape of mammalian teeth, potentially influencing diet. Mammalian tooth development is thought to proceed by an ‘inhibitory cascade’, whereby the growth of each developing tooth is controlled by a balance between stimulatory signals from the embryonic tissue, and inhibitory signals from the adjacent tooth. This results in the middle molar being intermediate in size between the first and last molar.

Coloured teeth

Lower right jaw of two early mammals, showing the first molar (yellow), second molar (green) and third molar (red).
Pentacodon occultus (left) – a very early insectivorous mammal
Hyracotherium (right) – the first horse, a browsing herbivore
Photograph by Thomas Halliday

Across 154 species of mammal, despite considerable variation in tooth shape and size, the relative sizes of the three molars conformed to the same basic pattern in about two thirds of species. The largest tooth was almost always either the first or last molar, in line with a common pattern of tooth development across all mammals. Diet is strongly related to tooth size and shape: mammals with a larger third molar (coloured red) tend to eat more plant matter, while mammals with a larger first molar (coloured yellow) tend to be meat-eaters. Across 180 million years of evolution, almost all mammals still conform to the same basic pattern of tooth development that their early ancestors used.

The Exception to the Rule
One extinct group of mammals, called condylarths, bucked the trend in molar shape. Their middle molar was largest, inconsistent with an inhibitory cascade. Perhaps this was an archaic adaptation to a new diet – condylarths were among the first omnivorous mammals, and a similar pattern is found in modern-day bears. The developmental constraint of the may not have been too strong for this particular deviation, though, and could have been achieved by a fairly simple modification to the inhibitory cascade.

Adaptation is not infinitely plastic. Natural selection can only work with the raw materials of variation in the population. Sometimes, one aspect of life constrains another, but if the pay-off is great enough, evolution will often find a way, despite the constraints.

Original Articles:

()Testing the Inhibitory Cascade Model in Mesozoic and Cenozoic Mammaliaforms BMC Evolutionary Biology 13: 79


This project was made possible by funding from the Natural Environment Research Council (NERC), as well as Abbey Research and Collaboration Awards and the University of London Central Research fund.