How we got here: evolutionary changes in skull shape in humans & their ancestors.
Abstract: This activity uses inquiry to investigate how large changes in shape can evolve from small changes in the timing of development. Students measure skull shape in fetal, infant, juvenile, and adult chimpanzees and compare them to adult skulls of Homo sapiens, Homo erectus, and Australopithecus afarensis. They conclude by re-interpreting their findings in light of Ardipithecus ramidus.

Key Words: Macroevolution; human evolution; heterochrony; development; chimpanzee; Ardipithecus ramidus; hypothesis testing.
Article Type: Report
Subject: Fossil hominids (Physiological aspects)
Human evolution (Study and teaching)
Sciences education (Methods)
Skull (Physiological aspects)
Author: Price, Rebecca M.
Pub Date: 02/01/2012
Accession Number: 278881935
Full Text: Although macroevolutionary processes are traditionally overlooked in introductory biology courses (Catley, 2006), they are essential for overcoming a number of misconceptions (Padian, 2010). This activity offers one way to teach students about macroevolution by demonstrating that variation in the development of individuals is fodder for large changes in shape.

Although intended for AP Biology and college students, one approach for adapting this exercise for high school is presented in Appendix A. The whole exercise takes first-year college students between 2 and 4 hours of class time to complete. Students test the hypothesis that different species of hominins evolved by retaining the juvenile characteristics of a chimpanzee-like ancestor and then reconsider their hypothesis in light of the recent discovery of the nearly complete skeleton of Ardipithecus ramidus (Gibbons, 2009; Lovejoy, 2009), which questions the idea that chimpanzees retain an ancestral shape.

I use the Biological Sciences Curriculum Study "5E" model (Bybee, 1997) to frame the activity. Sections are labeled Engage, Explore, Explain, Elaborate, or Evaluate to indicate their stage in this inquiry-based learning cycle. Students focus especially on hypothesis testing and revision, which fall into the explain-elaborate-evaluate stages.

* Materials

The activity requires line drawings (Figures 2 and 4), casts of skulls (Table 1), or a combination of both. Students gain more from the exercise when they handle casts (Thomson & Beall, 2008), but casts are expensive. Instructors may consider purchasing one or two skulls to supplement the line drawings, perhaps building a collection over several years. The students will also need graph paper, rulers, and calipers.

Learning Goals

By completing this exercise about the role that developmental timing has in evolution, students will

* recognize that developmental changes in shape are a source of heritable variation upon which evolutionary processes can act (Engage, Explore, Explain).

* recognize that evolutionary change results in a mosaic of primitive and specialized characteristics within each species (Engage, Explore, Explain).

* test the hypothesis that hominins evolved by retaining some juvenile characteristics of their ancestors, but also by extending the growth of other characteristics (Explain, Elaborate, Evaluate).

* practice scientific inquiry by collecting data, constructing, and interpreting graphs, and using their results and new data to test and revise a hypothesis (Engage, Explore, Explain, Elaborate, Evaluate).

* Engage: Discovering Changes in Shape during Development

In a homework assignment designed to engage students with the idea that organisms undergo large changes in shape as they grow, students conduct an Internet search about the axolotl, a Mexican salamander that reaches adulthood without undergoing metamorphosis (Zimmer, 1998). The students sketch an adult axolotl and write a brief explanation of why the adult looks juvenile. Their explanations should communicate that the timing of development has changed such that the adult axolotl retains the juvenile features even though it reaches sexual maturity. (Because this is an Internet search, an opportunity for addressing information literacy exists; sometimes, I ask students how they determined whether the sources they used were appropriate.) I also ask students to think of other organisms that change shape during development (like dogs) in addition to ones that grow without changing shape (like cats).

The homework assignment concludes with a brief introduction to the work we will do in class. I tell students that we will study chimpanzees (Pan troglodytes), anatomically modern humans (Homo sapiens), and the extinct species Australopithecus afarensis and Homo erectus. I explain that we will test the following hypothesis: Evolution of skull shape within the human lineage took place largely by changing the timing of events in development from a chimpanzee-like ancestor. To assess whether the students understand the hypothesis, I use an online adaptation of a minute-paper for assessment: each student sends me an e-mail message that paraphrases the hypothesis and justifies why it is worth testing.

When we meet in the classroom, we review the tenets of natural selection: that heritable variation exists in a population, that more offspring are born than can survive, and that individuals compete for survival. Students then relate those tenets to the changes they see in the development of the axlotl. They should realize that the change in shape during development (that is, allometry) is a source of heritable variation that can lead to survival of the fittest. This understanding helps students see that large amounts of variation already exist in the genome.

This activity focuses on morphology and not genetics, but it helps students to understand that these two biological disciplines are united by evo-devo (Carroll, 2005). In class, I briefly mention to students that growth from fertilized egg to adult involves a host of complex interactions among genes, molecules, and tissues. Subtle alterations in the time at which one of the genes responsible for these interactions is expressed can have far-reaching consequences that result in a different adult shape (Carroll, 2005). I return to this concept at other points during the term.



* Explore: Specimens

The next step in the activity is for students to gain a qualitative understanding of the developmental changes that humans and chimpanzees undergo (Figures 1 and 2) and to place this understanding in the context of their hypothesis. Students work in pairs to analyze the changes in shape that humans undergo from shortly after fertilization to adulthood (Figure 1). They list a series of traits that differ across the developmental stages, such as head-to-body size, leg-to-body size, eye-to-head size, and belly-button-to-body size.

Then students analyze the way chimpanzee skulls change shape during development (Figure 2). I ask pairs to identify 5-10 features that they could measure to describe the changes in shape they observe.

At this point, students need a quick digression to contemplate the difference between shape and size. I present students with a dilemma: how do they compare the size and shape of a toy car and a real car? Through discussion, they realize that comparing the lengths reveals information about the size but does not say anything about shape. On the other hand, comparing the ratios of length to height does record information about shape. I mention that this mathematical tool is called standardization and that the students will need to decide what to use to standardize their measurements. To assess their understanding of this concept, I ask students to explain how Figure 1 illustrates standardization; they should note that size has been removed from the drawing by scaling all three developmental stages to the same length.

Now the pairs of students have an inkling of the data they can use to test their hypothesis. This exploration concludes by changing that inkling into explicit understanding: students construct concept maps that illustrate what the hypothesis predicts and how the features of the skull that they identified provide evidence to test those predictions (Figure 3).



* Explore: Collect & Present Data

Student pairs choose two of the measurements that they identified to take on the skulls to quantify shape and one measurement to use to standardize the others. In addition to measuring the chimpanzee skulls (Figure 2), they should also collect data from the three adult hominins (Figure 4). They record the measurements in a table, calculate the standardized measurements, and then graph the results in a bivariate plot (see Appendix B for examples of measurements, table, and graph).

In my experience, students automatically try to fit a curve to the data without thinking about what a curve means. Here, a curve represents a developmental sequence, so it makes sense to add a best-fit curve to the points representing different stages in chimpanzee development. If students choose sexually dimorphic measurements, they may have one curve for the female chimpanzee and another for the male. Students generally need to be reminded that the points for A. afarensis, H. erectus, and H. sapiens are not part of any curve because they represent only the end points of different developmental sequences.

* Explain & Elaborate: Investigate the Data

Now students are ready to analyze their results. Questions like the following help them interpret their data as evidence to support or reject their hypothesis.

1. Use your graph to compare the chimpanzees and the hominins. How does skull shape change along the horizontal axis? How does shape change along the vertical axis?

2. Do the hominins fall above, below, or on top of the curve representing the development of the chimpanzee? Why?

3. Which stage of chimpanzee development is most similar to that of A. afarensis? to H. erectus? to H. sapiens?

4. Which hominin species is most similar to an adult chimpanzee?

5. Based on the information provided in Figure 1, what do you think the curve representing the development of humans would look like?

6. Do you accept or reject the hypothesis that you tested? Why?

* Elaborate & Evaluate: New Data from Ardi

Introducing Ardi (Ardipithecus ramidus) at the end of this activity models a small paradigm shift for students. The hypothesis they tested assumed that the hominin ancestor resembled chimpanzees, and that assumption was quite common among paleoanthropologists until recently (Lovejoy, 2009). But Ardi lived close to the time that our lineage diverged from chimpanzees, and she represents a mosaic of primitive and derived traits. Ardi gives us very good evidence that, in fact, chimpanzees are fairly specialized, and that our species retains a host of primitive traits (Lovejoy, 2009). Small teeth like ours, indicative of a generalized diet, are older than the large teeth chimps use for grinding food (Lovejoy, 2009). Ardi, like Homo sapiens, did not have the extreme sexual dimorphism of chimpanzees (Lovejoy, 2009), and she also had limbs shaped more like ours than like chimps' (Lovejoy et al., 2009). Ardi's skull also shares features with ours: it is relatively narrow and the spinal column entered the skull toward the center of its base, as it does in other bipedal apes. An artist's rendering of Ardi's skull can be easily obtained through the Internet (see Gibbons, 2009; accessible with free registration on the Science website or conduct an image search on "Ardi").

Still working in pairs, students analyze a drawing of Ardi's skull and add her to their graphs. Then, using a table of the ages of crucial events in hominin evolution (Table 2), I ask the students to infer how hold Ardi is. Students can guess that something is amiss, so I remind them to justify their inferences instead of simply guessing. After they articulate their hypotheses, I tell them that Ardi is 4.4 million years old (Gibbons, 2009), and I explain that she is a mosaic of primitive and derived features. As a class, we revisit the hypothesis that we tested, noting the assumption that chimpanzees had an ancestral shape, and acknowledge that, as written, we have to reject our hypothesis. Then, student pairs develop a new hypothesis that is consistent with the data and specify the kind of additional information they would need to test their new hypothesis. Astute students will recognize that chimpanzees have actually extended their development (they undergo more shape change before reaching sexual maturity--peramorphosis; Gould, 1977), whereas humans have shortened their development (we undergo less shape change by the time we reach maturity--paedomorphosis; Gould, 1977).

* Evaluate: Summative Assessment

I have included ideas for formative assessment throughout this description so that instructors can identify and correct students' misconceptions during the activity. However, a number of summative assessments help drive home the crucial points:

1. Show students a cast or drawing of Piltdown Man (Gould, 1980) and ask them whether this fossil is ancestral to hominins. They should be able to tell that the cranium is a Homo sapiens. Students thoroughly enjoy learning about the Piltdown controversy.

2. Ask students to outline the activity as they would a scientific paper, with Introduction, Materials and Methods, Results, and Discussion.

3. Conduct pre- and postdiagnostic tests of macroevolution using the Measure of Understanding of Macroevolution (Nadelson & Southerland, 2010).

4. Although the procedures in this activity are typical of those that paleobiologists make in their professional work, this activity makes some simplifications so that it can be completed in class. Ask students to identify some of these simplifications.


DOI: 10.1525/abt.2012.74.2.8

Appendix A: Adjustments for High School

Here is one way to adapt this exercise to a 50-minute high school session:

1. Engage: assign homework that introduces students to the axlotl.

2 Explore: pairs of students analyze the changes in shape that humans experience during development (Figure B1).

3. Explore and explain: pairs arrange cutouts of the chimpanzee skulls from youngest to oldest; ask students which traits they used to make their decisions.

4. Explore and explain: ask students which stage of chimpanzee development looks most like a human skull; help them justify their answers. Guide them toward the observation that modern humans look like juvenile chimpanzees.

5. Explore and evaluate: ask "if modern humans look like baby chimpanzees, which stage in chimpanzee development will Homo erectus look like?" Show them Homo erectus and have them evaluate their prediction. Repeat with Ardi.

Appendix B: Sample Results


* Acknowledgments

This activity was inspired by one written by David Jablonski and Michael Foote. Anne Sanford (Cleveland Museum of Natural History) provided a cast of a juvenile chimpanzee skull. William H. Leonard, Charlotte Rasmussen, Carrie Tzou, and three anonymous reviewers offered several helpful suggestions. I thank Mark Terry for encouraging me to write this article.


Bybee, R.W. (1997). Achieving Scientific Literacy: From Purposes to Practices. Portsmouth, NH: Heinemann.

Carroll, S.B. (2005). Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom. New York, NY: Norton.

Catley, K.M. (2006). Darwin's missing link--a novel paradigm for evolution education. Science Education, 90, 767-783.

Gibbons, A. (2009). A new kind of ancestor: Ardipithecus unveiled. Science, 326, 36-40.

Gould, S.J. (1977). Ontogeny and Phylogeny. Cambridge, MA: Harvard University Press.

Gould, S.J. (1980). Piltdown revisited. In The Panda's Thumb: More Reflections in Natural History (pp. 108-124). New York, NY: Norton.

Lovejoy, C.O. (2009). Reexamining human origins in light of Ardipithecus ramidus. Science, 326, 74, 74e1-8.

Lovejoy, C.O., Suwa, G., Simpson, S.W., Matternes, J.H. & White, T.D. (2009). The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes. Science, 326, 100-106.

Moore, K.L. & Persaud, T.V.N. (1993). The Developing Human: Clinically Oriented Embryology, 5th Ed. Philadelphia, PA: Saunders.

Nadelson, L.S. & Southerland, S.A. (2010). Development and preliminary evaluation of the Measure of Understanding of Macroevolution: introducing the MUM. Journal of Experimental Education, 78, 151-190.

Padian, K. (2010). How to win the evolution war: teach macroevolution! Evolution: Education and Outreach, 3, 206-214.

Thomson, N. & Beall, S.C. (2008). An inquiry safari: what can we learn from skulls? Evolution: Education and Outreach, 1, 196-203.

Zimmer, C. (1998). At the Water's Edge: Macroevolution and the Transformation of Life. New York, NY: Free Press.

REBECCA M. PRICE is Assistant Professor of Interdisciplinary Arts and Sciences at the University of Washington, Bothell, Box 358530 18115, Campus Way NE, Bothell, WA 98011-8246; e-mail:
Table B1: Measurements of distances graphed in Figure B1.

Skull                        w (mm)    jc (mm)   ht (mm)   w/ht   j/ht

Fetal chimp                   64.27     15.63     52.86    1.22   0.30
Infant chimp                  93.40     23.16     77.06    1.21   0.30
Juvenile chimp               109.85     35.05     86.97    1.26   0.40
Adult female chimp           120.17     49.17     89.47    1.34   0.55
Adult male chimp             116.70     50.29     84.76    1.38   0.59
Australopithecus afarensis    93.62     20.19     79.22    1.18   0.25
Homo erectus                 129.88     27.77     95.66    1.36   0.29
Homo sapiens                 112.79     24.85     99.83    1.13   0.25
Ardipithecus ramidus         249.76     70.73    167.96    1.49   0.42

Table 1. Casts of skulls in this activity.

Skull                         Manufacturer

Fetal chimpanzee              Bones Clones

Infant chimpanzee             Bones Clones

Juvenile chimpanzee           Cleveland Museum of
                              Natural History
                              (specimen B1437)

Female adult chimpanzee       Bones Clones

Male adult chimpanzee         Bones Clones

Adult Homo sapiens            Bones Clones

Adult Homo erectus            Bones Clones

Australopithecus afarensis    Bones Clones

Ardipithecus ramidus (Ardi)   Bones Clones

Table 2. Important dates in hominin evolution.
Dates from Gibbons (2009) and Lovejoy et al.

Chimpanzee--hominin divergence   5-6 million years ago
Australopithecus afarensis       3.7 million years ago
Homo erectus                     1.8 million years ago
Homo sapiens                     40,000 years ago