Developmental Constraints, Genetic Correlations & Natural

Selection

Genetic Constraints Arise From Pleiotropy and Epistasis

When the above equation is not zero and contains a non-zero covariance term, evolution at the multi-trait level is often non-optimal in the sense that not every trait, or even no traits, are at their optimal value.

In this sense, many regard constraints and genetic correlations as interfering or limiting adaptive evolution via natural selection.

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∂2w(xeq ,yeq )

∂x 2σ eq

2 (x) + 2∂ 2w(xeq ,yeq )

∂x∂yCoveq (x,y) +

∂ 2w(xeq ,yeq )

∂y 2σ eq

2 (y)

Even when correlated traits are “optimized”, the genetic correlations due to pleiotropy often can cause a “non-optimal” trajectory (Guillaume, F., and M. C. Whitlock. 2007. Evol. 61:2398-2409):

Evolutionary trajectory: each dot = mean in successive generations

Do Constraints Overwhelm or Inhibit Adaptive Evolution via

Natural Selection?

Wagner GP (1988) The influence of variation and of developmental constraints on the rate of multivariate phenotypic evolution. Journal

of Evolutionary Biology 1, 45-66.

Wagner GP (1988) The influence of variation and of developmental constraints on the rate of multivariate phenotypic evolution. Journal

of Evolutionary Biology 1, 45-66.

If high fitness depends upon 3 or more integrated traits, and all traits are genetically independent, the integrated state is unlikely to evolve.

There is a greater chance of multi-trait evolution even under random patterns of pleiotropy and epistasis!

Genetic Correlations Among Traits Are Also a Phenotype That Can Be Influenced By Genetic Variation and Therefore Can Evolve

Hansen TF (2006) The evolution of genetic architecture. Annual Review of Ecology Evolution and Systematics 37, 123-157.

Simulations showed that epistasis can constrain adaptive responses (green lines), but in other cases can greatly facilitate them (red lines).

Recall, like in coalescence theory, what we see today are the successful lineages, so Hansen argues that constraints due to epistasis have facilitated adaptive change.

Ciliberti S, Martin OC, Wagner A (2007) Innovation and robustness in complex regulatory gene networks. PNAS 104, 13591-13596.

Interaction networks with redundancy create robustness, but can sometimes lead to high innovation and sometimes lead to evolutionary stasis.

Genetic Redundancy & Innovation: Gene Duplication Followed By Divergence Yields Families of Functionally Related Genes

Genetic Redundancy & Innovation: Developmental Modularity

Wagner GP, Altenberg L (1996) Perspective - Complex Adaptations and the Evolution Of Evolvability. Evolution 50, 967-976.

Genes

Character Complexes

Functions

Genetic Redundancy & Innovation: Developmental Modularity

Evolution of diverse functions from modular traits.

Genetic Redundancy and Developmental Modularity Give Life the Potential for Robustness

and Innovation.Can Sometimes Lead to Stasis and

Maladaptations, but In Some Cases Constraints are Facilitators of Adaptive Evolution

Pigliucci M (2008) Is evolvability evolvable? Nat Rev Genet 9, 75-82.

Within species

Within species, the right balance of interaction, redundancy, and developmental constraints interacts with selection to open new areas of phenotypic space for further evolution

Example: Anolis lizard species in the Caribbean

Numbers of Species on Various Islands

Anolis lizard species on different islands show similar morphological

adaptations associated with similar habitats.

Grass/Bush Habitat

Specialist

Trunk/Ground Habitat Specialist

Trunk/Crown Habitat Specialist

Twig Habitat Specialist

Species Adapted to the Same Habitat On Different Islands Look Similar Whereas

Species Adapted to Different Habitats On the Same Island Look Very Different

Puerto Rico

Jamaica

Hypothesis:The Transitions in Development

Associated With the Various Habitat Specialists Are So Difficult

To Evolve, That They Probably Only Evolved Once.

The Comparative MethodPROBLEM: When

Evolutionary Trees Were Constructed From

Morphological Traits, The Tree Could Only Be

Constructed By Making Assumptions About the

Evolution of Morphological Traits.

The Comparative MethodSolution: George Gaylord Simpson, 1945:

The most direct, but unfortunately not the most useful, approach to the phylogeny of recent animals is through their genetics. The stream of heredity makes phylogeny; in a sense, it is phylogeny. Complete genetic analysis would provide the most priceless data for the mapping of this stream, . . . and the advantage of genetics lies . . . in the fact that the genes . . . are the immediate physical continuants of phylogeny, while morphology is less direct, a result of those hereditary factors as modified by other influences.

Ancestral Reconstruction of Habitat Specialist Evolution on

Two Islands

Twig

Jamaica

Twig

Puerto Rico

Generalist Generalist

Ancestral Reconstruction of Habitat Specialist Evolution on

Two Islands

TwigTrunk/Ground

Jamaica

Twig

Puerto Rico

Crown/Giant

Trunk/GroundCrown

GeneralistGeneralist

Ancestral Reconstruction of Habitat Specialist Evolution on

Two Islands

TwigTrunk/Ground

Jamaica

Twig

Puerto Rico

Crown/Giant

Trunk/Ground

Crown/Giant

Trunk/Crown

Trunk/Crown

Crown

GeneralistGeneralist

Trunk/Grnd

Ancestral Reconstruction of Habitat Specialist Evolution on

Two Islands

TwigTrunk/Ground

Jamaica

Twig

Puerto Rico

Crown/Giant

Trunk/Ground

Crown/Giant

Trunk/Crown

Trunk/Crown

Grass/Bush

Crown

GeneralistGeneralist

Trunk/Grnd

Trunk/Grnd

Ancestral Reconstruction Implies Great Evolutionary Flexibility

Twig

Puerto Rico

Crown/Giant

Trunk/Ground

Trunk/Crown

Grass/Bush

Generalist

Trunk/Grnd

Trunk/Grnd

Reject Hypothesis of Developmental Rigidity: The

Developmental System Leading To Basic Body Shape

and Limb Morphology in Anolis lizards Shows Great

Evolutionary Flexibility And Evolves Repeatedly In Response To Habitat

Availability Upon Each Island

Genes Can Influence the Timing and Duration of

Processes, Which Can Lead to Much Phenotypic Innovation In

A Developmentally Constrained System.

The Human Brain

Humans achieve their large brains in part by retaining the normal primate brain growth processes, but start them earlier and retain them longer.

The Human Brain

Humans achieve their large brains in part by retaining the normal primate brain growth processes, but start them earlier and retain them longer.

Chimpanzee

Human

The Human Brain

Humans retain fetal and newborn growth

processes over a longer portion of their life.

Pleiotropy: Not All Traits That Evolve Under Natural Selection Are Adaptive.

The Human Jaw Is Too Small For Its Teeth, Leading to Complications in Arrangement and “Wisdom Teeth.”

Selection Operates Through the Genetic System Upon

Developmental Processes (as judged from the gamete’s average

perspective) and Not Upon Isolated Traits.

Much of Evolution Is Therefore Non-Adaptive or Even Mal-Adaptive Even

When Driven by Natural Selection (Recall Sickle Cell Anemia).

When traits are neutral but developmentally correlated to a

selected trait, we expect its evolution to obey those correlations.

When two or more developmentally correlated traits are separately

selected, we expect deviations from the expected developmental

correlations in their joint evolution.

Example, human face and jaws

A Quantitative Genetic Overlay Upon Facial Morphology Using Modern Humans, Chimps and Gorillas as Models Revealed A Relaxation of

Selection On The Face and Jaws in the Human Lineage, Indicating A Significant Increase in Reliance Upon Culture & Tools (Ackermann &

Cheverud, PNAS 101: 17946, 2004)

Constraints Insure That Much Phenotypic Evolution is

Neutral or Even Maladaptive; but Population Genetic Theory

Indicates that Epistasis and Pleiotropy Can Sometimes Be Strong Facilitors of Adaptive

Innovation.