The tree of life provides a fundamental roadmap to understanding biodiversity, yet requires integration across scales of the biological hierarchy and a unique set of tree thinking skills. This combination can be challenging for undergraduates at the introductory level because of their preconceptions regarding distinct fields of biology compounded by the unique structure of phylogenetic trees. To address these two challenges while providing an undergraduate research opportunity, we developed an activity for introductory biology students that integrates molecular, organismal, and evolutionary biology. This activity relies on woody plant identification, comparative morphology, and DNA sequence analysis to teach students how to reconstruct and interpret phylogenetic trees. After building separate phylogenetic hypotheses using morphological characters and molecular data, they compare their results with a master Tree of Trees to identify instances of homology and homoplasy. After delivering this activity, the majority of students scored the activity as “helpful to very helpful” in increasing their understanding of these concepts. Overall, we deliver a framework for developing comparable Tree of Trees–type activities that leverage students' interests in familiar organisms and requires them to span scales of the biological hierarchy while improving their tree thinking skills.

The affinities of all the beings of the same class have sometimes been represented by a great tree … As buds give rise by growth to fresh buds, and these if vigorous, branch out and overtop on all sides many a feebler branch, so by generation I believe it has been with the great Tree of Life, which fills with its dead and broken branches the crust of the earth, and covers the surface with its ever branching and beautiful ramifications. (Darwin, 1859)

Introduction

Evolution's tree of life provides a fundamental roadmap to understanding biodiversity (Hinchliff et al., 2015). In Darwin's “great tree” quote, he integrates numerous sub-disciplines of biology, including taxonomy (“same class”), phylogenetics (“great tree”), inheritance (“buds give rise to fresh buds”), paleontology (“dead and broken branches”), and natural selection, the hallmark of evolutionary biology (Darwin, 1859). Phylogenetic trees are now used across an even broader set of disciplines in biology: understanding biodiversity (Hinchliff et al., 2015; Maddison & Schulz, 2007), tracing the history and transmission of diseases (Worobey et al., 2008), understanding the fate of cell lineages (Salipante & Horwitz, 2006; Sulston et al., 1983), criminology (Scaduto et al., 2010), and more (Cracraft & Donoghue, 2004). Phylogenetic systematics, a worldview born from Darwin (1859) and formalized by Hennig (1966), dictated the transition from ladder thinking to tree thinking (O'Hara, 1988). Despite the existence of national Next Generation Science Standards—which expect graduating 12th graders to understand phylogenetic concepts such as common ancestry, branching patterns of relatedness, and how similarities in DNA sequences and anatomical structures reflect phylogenetic relationships (National Academy of Sciences, 2012)—chronic evolutionary misinterpretations of phylogenetic trees persist even among college-level biology students (Gregory & Ellis, 2009; Phillips et al., 2012). Tree thinking (O'Hara, 1988; Baum et al., 2005) requires intentional learning activities (Brown, 2016) to counter a history of phylogenetic confusion and misunderstanding (Sandvik, 2008; Halverson, et al., 2011).

Learning to correctly interpret phylogenetic trees presents a unique set of challenges. Although often introduced as graphs with a time axis, the perpendicular axis typically has no units with arbitrary spacing that is more aesthetic than quantitative (Meisel, 2010). Further complications arise from the urge to “read the tree” from left to right and top to bottom, when in fact it should be read by following the pathways of the branching events from the root to the tips or vice versa (Sandvik, 2008; Meir et al., 2007). The ability to rotate branches without changing the meaning of the tree (but never translocating branches) is another challenge to students (Halverson, 2010). Halverson et al. (2011) developed an eight-step progression in tree thinking skills for a course in plant systematics in which only the “expert professor” was able to ascend to the eighth level!

How the tree is drawn, in both shape and direction, can affect student learning. Pedagogical studies of tree interpretation indicate that bracketed trees with right angles at the nodes (instead of diagonally drawn trees) increase students' comprehension (Novick & Catley, 2007; Novick et al., 2012). Furthermore, psychological studies of phylogenies drawn with the common ancestor on the left and that appear to branch in a downward fashion is the format that accommodates the inherent tendencies of student eye movements (Novick et al., 2012). Collectively, the unique way in which phylogenetic trees are drawn and interpreted requires an intentional set of activities to develop students' tree thinking skills (Meir et al., 2007; Perry et al., 2008; Baum & Smith, 2012).

To give students practice in building and comparing phylogenetic trees, we developed a discussion activity for introductory bioscience students that integrates molecular, organismal, and evolutionary biology utilizing tree diversity (hereafter referred to as “woody plants” to avoid confusion). Woody plants represent many diverse branches of the plant tree of life and exhibit fascinating adaptive traits that reflect the range of evolutionary scenarios, including instances of homology and homoplasy (i.e., reversals and convergence) (Ritter, 2011; Smith & Donoghue, 2008). We have chosen to teach phylogenetics by reconstructing and comparing phylogenies of woody plants on campus because of their familiarity among undergraduate student population and their reliability for teaching purposes (once identified, they are very likely to be there in the future). By using dichotomous keys, students are prompted to assess morphological traits and thereby invest in a self-selected set of trees for reconstructing their phylogenies.

Throughout the activity, we have decided to use scientific names because of the ambiguity associated with some common names (e.g., “primrose” can be applied to an herbaceous annual and a woody perennial, both of which are present on our campus). The primary goal of this phylogenetics module is to deepen students' understanding of how to build and compare phylogenetic trees. A secondary goal is to introduce them to campus woody plant diversity and to provide them with exposure to basic natural history training lacking in today's student body (Louv, 2005). Through first-hand experience constructing and analyzing phylogenetic trees with real data, students gain a deeper evolutionary understanding by going beyond textbook examples and playing with imaginary organisms (Brown, 2016; Hillis et al., 2013; Maier, 2001).

Learning Objectives

This activity strives to span traditionally disparate fields of biology from molecules to organisms to macroevolution. By the end of this activity, we expect students will be able to:

  • Identify organisms by navigating a dichotomous key.

  • Use morphological characters and DNA sequences to develop phylogenetic hypotheses using parsimony.

  • Compare phylogenetic trees built with different sources of data.

  • Recognize macroevolutionary phenomena such as homology and homoplasy.

Creating the “Tree of Trees”

Although we recognize that some of the details of this activity are site-specific, we endeavored to develop a novel framework for leveraging students' familiarity with their surroundings as a starting point to transcend traditionally distinct subdisciplines of biology. We focused on a region of Santa Clara University's campus that contains a particularly diverse assemblage of trees. After identifying the majority of woody species, including trees, shrubs, and vines, we found 67 woody species, including one fern, 12 gymnosperms, and 54 angiosperms. Within the angiosperms were 11 monocots and 43 eudicots. Then, we developed a custom dichotomous key to assist students with species identification (Online Supplemental Material, Appendix 1) by modifying and supplementing an existing key to urban trees of California (Ritter, 2011). The key was developed for amateurs to successfully identify trees without technical jargon while avoiding any specialized equipment (i.e., no hand lens necessary), and including images of relevant characteristics.

To offset the additional time investment on the instructor's part, the tree identifications, dichotomous key, and DNA sequence retrieval and comparisons were done largely by an upper division biology student (the first author) as an independent research project. The bulk of the activity materials were the project's main outcomes, simultaneously providing an undergraduate research opportunity while helping the instructor create original deliverables. This method could also be utilized at other institutions to benefit instructors, introductory bioscience students, and upper division research students alike.

To illustrate evolutionary relationships for all woody taxa, we chose to use 18S ribosomal DNA because of the large amount of available data. The sequences for all taxa or their closest relatives were retrieved from Genbank (Online Supplemental Material, Appendix 2) and aligned. For 52 percent of the taxa (35/67), we found 18S rDNA sequences for the exact same species as we identified on campus. For another 19 percent of the taxa (13/67), we used the closest, available representative from the same genus. For the remaining taxa (37%, 19/67), we used sequences from the closest representative from the same family. They were aligned with the default settings in ClustalX in Geneious v. 8.1.7 (Kearse et al., 2012) producing a 1,614 bp alignment available by request (see Figure 1 for portion of the alignment for a subset of trees).

Figure 1.

A portion of the 18S alignment for a sample of tree species on campus. Major lineages are indicated with brackets. For species with no available sequences, we used the closest relative with an available 18S sequence as indicated with parentheses.

Figure 1.

A portion of the 18S alignment for a sample of tree species on campus. Major lineages are indicated with brackets. For species with no available sequences, we used the closest relative with an available 18S sequence as indicated with parentheses.

The master SCU Tree of Trees was built using maximum likelihood (GTR+CAT+I parameter settings with 1000 bootstrap replicates) in RAxML (Stamatakis, 2014) and is largely congruent with our current perspective on angiosperm relationships (Figure 2) (Stevens, 2017. In addition, each taxon was scored for several morphological traits, including reproductive mode and fruit type. These traits were then mapped onto the master Tree of Trees using parsimony in Mesquite (Maddison & Maddison, 2016) to demonstrate evolutionary patterns in the plant tree of life (Figure 3). In particular, we focused on the evolution of reproductive mode (flowers or cones) and fruit type (dry or fleshy) to demonstrate two contrasting patterns of character evolution (see Online Supplemental Material, Appendix 2, for character coding). For reproductive mode, there is a single shift from cones to flowers along the branch leading to the angiosperms, clearly indicating homology (Figure 3A). Alternatively, for fruit type there are 15 transitions scattered throughout the tree with several instances of homoplasy (i.e., convergence and reversal) (Figure 3B).

Figure 2.

Maximum likelihood phylogenetic analysis of 67 SCU campus trees based on 18S DNA sequence data. Asterisks above branches indicate bootstrap values >70%. Species names in parentheses are the Genbank samples used as placeholders when 18S sequences were unavailable for that particular species. Major lineages are identified with arrows. Selected woody trees are represented with images from campus.

Figure 2.

Maximum likelihood phylogenetic analysis of 67 SCU campus trees based on 18S DNA sequence data. Asterisks above branches indicate bootstrap values >70%. Species names in parentheses are the Genbank samples used as placeholders when 18S sequences were unavailable for that particular species. Major lineages are identified with arrows. Selected woody trees are represented with images from campus.

Figure 3.

Ancestral state reconstructions of reproductive traits for the 67 SCU campus trees. Reproductive mode (cones versus flowers) is homologous (A), whereas the evolution of fruit types (dry versus fleshy) is homoplasious because of convergence and reversals (B). When the trait is not applicable to particular tree species (such as the outgroup), those branches are treated as missing data and are indicated by dark grey branches in both A and B.

Figure 3.

Ancestral state reconstructions of reproductive traits for the 67 SCU campus trees. Reproductive mode (cones versus flowers) is homologous (A), whereas the evolution of fruit types (dry versus fleshy) is homoplasious because of convergence and reversals (B). When the trait is not applicable to particular tree species (such as the outgroup), those branches are treated as missing data and are indicated by dark grey branches in both A and B.

The phylogenetic tree, along with the DNA sequences and dichotomous key, was then integrated into a discussion activity for an introductory biology course in ecology and evolution. After delivery of this tree thinking activity, we assessed its ability to improve tree thinking using student narrative evaluations and student performance on selected final exam questions.

Teaching Tree Thinking with a Tree of Trees

The following steps describe a 65-minute discussion activity for a ten-week course entitled Introduction to Evolution & Ecology (4 units) for freshman biology majors, which includes three hours per week of lectures complemented by weekly discussion sections.

Figure 4.

Discussion activity flow diagram starts with a sampling of campus woody tree diversity identified with a dichotomous key (A). Then students create a table comparing morphological traits for their trees (B), and use this to build a morphology-based phylogenetic hypothesis (C). Morphological changes are indicated along the appropriate branches (C). Following the morphological analysis, students are given 18S DNA sequence data for their woody trees (D). They identify variable sites that are different from the outgroup (circled), and use these characters to build a molecular phylogenetic hypothesis with the changes indicated on the appropriate branches (E). Finally, students compare their phylogenetic hypotheses with the master “Tree of Trees” (F) requiring additional tree thinking skills to visualize the relationships of their samples within the context of the larger phylogeny (F).

Figure 4.

Discussion activity flow diagram starts with a sampling of campus woody tree diversity identified with a dichotomous key (A). Then students create a table comparing morphological traits for their trees (B), and use this to build a morphology-based phylogenetic hypothesis (C). Morphological changes are indicated along the appropriate branches (C). Following the morphological analysis, students are given 18S DNA sequence data for their woody trees (D). They identify variable sites that are different from the outgroup (circled), and use these characters to build a molecular phylogenetic hypothesis with the changes indicated on the appropriate branches (E). Finally, students compare their phylogenetic hypotheses with the master “Tree of Trees” (F) requiring additional tree thinking skills to visualize the relationships of their samples within the context of the larger phylogeny (F).

  1. In preparation for the discussion activity, each student identifies two trees or other woody plants in the designated area of campus using the dichotomous key (Online Supplemental Material, Appendix 1).

  2. Students bring in plant samples, cellphone images, or notecards with plant names, which are confirmed by the instructor(s) upon arrival (Figure 4A).

  3. In discussion, pairs of students analyze the morphological similarities among their four woody plants, this smaller set of species being easier to grasp and conceptualize (Randler & Bogner, 2002). The morphological data is used to generate a table based on the presence/absence of at least six traits (Figure 4B). Students use dry erase markers to write on pre-formatted, empty tables inserted into plastic cover sheets. Then, they use the table to develop a hypothesis of the relationships by circling shared characteristics that are distinct from the outgroup (synapomorphies), a tree fern (Figure 4C). We encourage them to start building their phylogenetic hypothesis by looking for sister species.

  4. Then, we provide students with an alignment of the first 21 variable sites of the 18S rDNA for their four taxa plus tree fern (Figure 4D) in a plastic cover sheet. Students then circle molecular synapomorphies with dry erase markers, and use this information to build a molecular phylogeny by hand, using parsimony (Figure 4E) and starting with sister species.

  5. After building their molecular tree, the students compare their trees with the master Tree of Trees (Figure 4F) to determine which method was more reliable. To help them compare their five species tree to the master Tree of Trees, we encourage our students to reduce the master Tree of Trees into a subtree that includes only their five species. To do this, we recommend they start at the tips asking, “Which of my five species are most closely related in the master Tree of Trees?” These become sister species in their subtree. From there, they can ask if there are more sister relationships, or if there are none, they can ask, “Which of my species is the next most closely related in the master Tree of Trees?” As the students build their subtree and begin comparing it to their morphological and molecular trees, it is critical they follow the lines of descent. We use the analogy of the branches as a tight-rope walk where you are only allowed to follow the line. We found this prevents the natural inclination to compare the species tips from left to right or top to bottom.

  6. Optional: After determining the most likely relationships based on the master Tree of Trees, it is beneficial for them to map the evolutionary history of their morphological traits (Step 3, above) onto the correct tree of five taxa to identify instances of homology and homoplasy (i.e., convergence and reversal). Students frequently struggle with how to interpret synapomorphies mapped onto phylogenetic trees (Dees et al., 2014), so we reserve this until the end, well after the phylogenetic tree is built.

Student Assessment Results

Although we did not conduct pre- and post-testing on students' tree thinking abilities, after our first trial with this activity, 72 percent of students scored the activity as “helpful to very helpful” in increasing their understanding of in-class, lecture material. Evaluation of studentfinal exams (n = 85) showed that students had higher performance on five tree thinking questions, including concepts of parsimony, synapomorphy, reversal, and relatedness (mean = 89.41 ± 1.56%; see Online Supplemental Material, Appendix 3, for examples), compared to 45 questions on other topics in ecology and evolution (mean = 84.03 ± 0.98%; paired t-test: n = 84, p = 0.0004). In future iterations, pre- and post-testing would help assess student learning more rigorously (possible questions are collected in Online Supplemental Material, Appendix 3).

Learning Outcomes

Professional scientists and instructors recognize the necessity to incorporate phylogenetics into biology courses, but the current educational system often emphasizes memorizing terminology rather than understanding core concepts (Goldsmith, 2003). In evolution instruction, there is an unbalanced focus on microevolution (Meir et al., 2007). Thus, cultivating students' tree thinking skills should improve their understanding of evolution and biology in general (Meisel, 2010). Although text books can properly illustrate evolutionary concepts (Hillis et al., 2013), and students can have a working understanding of these principles, an inquiry-based approach is needed to ensure that students are capable of creating their own accurate explanations of evolutionary phenomena, instead of falling back into habits of group and teleological thinking (Gregory & Ellis, 2009; Sandvik, 2008).

Our Tree of Trees activity was developed in an attempt to overcome these issues by leveraging organisms that students are familiar with because of their surroundings. Previous inquiry-based teaching methods, such as the Great Clade Race (Goldsmith, 2003) and computer simulations (Perry et al., 2008), take advantage of the peer instruction environment to demonstrate phylogenetic concepts that we have used as models in developing this activity. However, such activities have been shown to have little effect in improving certain erroneous concepts among students, such as reading trees and interpreting character evolution (Perry et al., 2008). In the Tree of Trees activity, students compare their five-taxa phylogeny derived from morphological and molecular analysis to the master phylogenetic tree of all woody plants, pushing them to practice tree thinking skills like trait mapping, tree pruning, and interpreting cases of homology and homoplasy. Another approach is to have students construct phylogenetic trees showing similarities between manufactured goods that they are familiar with, such as furniture (Nickels & Nelson, 2005). Unfortunately, the classification of manufactured goods does not demonstrate vertical descent from a common ancestor and seems like a missed opportunity to investigate biodiversity itself.

By taking advantage of readily available campus biodiversity, students use their own personal observations to develop phylogenetic hypotheses among living organisms, allowing them to practice their tree thinking skills with organisms they have personally invested in (Perry et al., 2008). The integration of a dichotomous key provides students with the tools necessary to explore natural history and cultivate their species identification skills. Identifying unknown organisms with six or fewer species, particularly with an identification book, has been shown to increase students' understanding of biodiversity and ability to recount species names and morphological characteristics (Randler & Bogner, 2002). With abundant diversity in tree species, students obtain a more realistic scientific experience when each team of students invests in a unique grouping of taxa and analyzes empirical data toward an unanticipated result. This presents more challenges, provides rigorous training in parsimony phylogenetics, and results in unique phylogenies throughout the class that would not be possible with simulated activities of prefabricated data. Complementing a morphological analysis with DNA sequence data helps to modernize the activity while emphasizing the multiple sources of evidence that can be brought to bear on macroevolutionary questions. Since DNA sequences usually evolve at similar rates amongst different lineages, simultaneous comparisons of these sequences will be less likely to lead students into thinking that one extant species is the ancestor of another extant species—a common misconception (Omland et al., 2008). The Tree of Trees activity introduces students to phylogenetic concepts with a more intuitive, character-based tree building, but leads to DNA sequence comparison to construct a phylogenetic hypothesis with strong emphasis on parsimony, an alternative to the genetic distance approach (Maier, 2001).

This interactive tree thinking activity can be adapted for introductory evolution and ecology students in various settings by similarly leveraging groups of organisms familiar to students and for which DNA sequence comparisons can be made. This activity could be modified for an advanced high school biology course since it addresses Next Generation Science Standards including common ancestry, phylogenetic trees, and comparing DNA sequences and anatomical structures to infer relatedness (National Academy of Sciences, 2012). Where campus tree diversity is too scarce for this activity, other groups of organisms can serve the same purposes of exploring natural history, comparing morphological traits, and analyzing molecular data. Campus bird diversity, insect diversity (perhaps at the level of family or order), and bacterial diversity are similarly tractable for such an activity. A comparable custom-made dichotomous key could be easily developed using resources for birds (Sibley, 2014) or insects (Choate, 2011; Powell & Hogue, 1980; Triplehorn & Johnson, 2005) for this or other locals. Students can derive morphological traits from comparing identified organisms, and after being provided with relevant DNA sequence data—18S rDNA in the case of birds and insects, or 16S rDNA in the case of bacteria—can proceed with constructing a molecular hypothesis. By studying living organisms, students can practice tree thinking and confront misconceptions through direct observation, interactive learning, and testing of empirical data, deepening evolutionary understanding and introducing them to the practice of scientific inquiry.

Suggestions for Future Teaching

To maximize the interactive learning experience, students benefitted most from working in pairs. For the Tree of Trees activity, each pair of students should have one gymnosperm, one or two monocots, and one or two eudicots to span the major evolutionary lineages. Pedagogical research on species identification by students suggests that eight to twelve species is a target sample size with which to start (Randler & Bogner, 2002). At the start of the phylogenetic tree building process, students may need to be prompted with morphological traits to compare, with leaf shape, leaf arrangement, overall architecture, and reproductive structures being among the most helpful. Furthermore, some students confused common names such as primrose (Primula vulgaris) and primrose tree (Lagunaria patersonia).

Since this activity gives each group an original, unique dataset, rather than premade data, more time may be required to allow students to fully analyze and map evolutionary traits for their chosen taxa, and the activity could easily be expanded to fill a standard university laboratory section (2–2.5 hours). The outcome of this learning module is not to focus on obtaining the “right answer,” but to urge students to develop tree building strategies and put tree thinking skills into practice. In the activity, students are prompted to find appropriate diagnostic morphological traits, analyze relative evolutionary proximity through ideas of synapomorphies and sister species, and practice of the concept of parsimony. The usage of real world data enables students to develop tree thinking skills that would otherwise be difficult to obtain from textbooks alone (Maier, 2004).

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