The behaviors of organisms evolve just as surely as do their physical features. Indeed, the connections between a species' behavioral repertoire and its suite of morphological attributes are almost always so tight as to blur distinctions between organismal form and function, i.e. between what a creature is and what it does. Adaptive co-evolution between a species' behavioral ecology and its physical attributes accounts for why we don't observe, for example, vegetarian leopards or predatory antelopes.

As presaged in Chapter 4, PCM analyses can be conducted on behavioral and lifestyle traits just as they can on morphological ones. This chapter will provide several additional examples ranging from evolutionary analyses of the kangaroo's bipedal hop to the organization of multi-species lizard communities on Caribbean islands, and from how pufferfish gained the ability to inflate their bodies into anti-predation balls to how particular bacteria sense the earth's geomagnetic field. In most of the following case studies, PCM analyses have been applied as well to anatomical attributes associated with particular organismal behaviors, meaning that the topics explored in this chapter will also overlap to some degree with those covered in Chapter 2.

The kangaroo's bipedal hop

When in fast gait, kangaroos and their relatives (family Macropodidae) employ the bipedal hop. Indeed, two-legged hopping is mandatory for rapid cross-country locomotion because these animals' forelimbs are short and weak whereas their long hindlimbs are powerfully constructed for propulsion.

The preceding chapters have dealt primarily with PCM studies of macroscopic external features – organismal morphologies, behaviors, and lifestyles – that are often readily visible to the observer's naked eye. This chapter will illustrate how comparative phylogenetic analyses can likewise be conducted on microscopic internal attributes such as an organism's molecular makeup, cellular functions, physiology, genetic mechanisms, or its intragenomic “microbial associates” (including viruses and transposable elements). We will consider, for example, what PCM has revealed about the evolutionary-genetic underpinnings of sex determination, of eye development, of metazoan (multi-cellular animal) body plans, and of cellular mechanisms for DNA repair. We will consider how various fishes evolved antifreeze proteins, the capacity to produce electrical currents, and warm-bloodedness. And we will track the recent evolutionary history of the HIV viruses that cause AIDS. In truth, almost any subject related to cellular biology, ranging from biochemistry to medicine and epidemiology, can be informed to one degree or another by comparative phylogenetic analyses.

Foregut fermentation

Most of the studies described in this book have employed molecular data as phylogenetic backdrops for interpreting the evolutionary histories of morphological or other organismal phenotypes. The general rationale, of course, is that, when species are assayed for hundreds or thousands of detailed genetic characters (as is typically the case with protein or DNA sequence information, for example), any widespread and intricate molecular similarities that might be observed are very unlikely to have arisen by convergent evolution, so they must instead reflect true phylogenetic descent.

Many recent textbooks (see References for Chapter 1) thoroughly cover the laboratory techniques of molecular genetics as well as phylogenetic methods of data analysis, at levels suitable, depending on the book, for readers ranging from novice to expert. Thus, this Appendix will confine its attention to some underlying concepts and methods specific to PCM per se. In other words, it is assumed for current purposes that appropriate molecular genetic data have been gathered and properly analyzed to estimate a robust phylogenetic tree for the taxa in question, and that the intent now is to map and interpret the distributions of particular phenotypes onto that tree. Normally, alternative states of phenotypic characters are known only for extant species (exterior nodes) of the phylogenetic tree; the goals of PCM are to infer ancestral character states at various interior nodes and to estimate character-state transitions along various tree branches. Only elementary aspects of PCM will be covered here. For far more complete and advanced treatments, including operational details, see Brooks and McLennan (1991, 2002), Eggleton and Vane-Wright (1994), Harvey and Pagel (1991), Harvey et al. (1996), Maddison and Maddison (2000), Page and Holmes (1998), and other references cited below.

History of cladistic concepts and terminology

Systematists from Aristotle to Linnaeus and beyond traditionally grouped organisms and erected biological classifications based on qualitative or quantitative appraisals of the overall resemblance (phenetic similarity) among taxa.

Many biologists now incorporate molecular phylogenetic analyses into their explorations of nature. Using sophisticated laboratory techniques, they uncover “DNA markers” or “genetic tags” that uniquely identify each creature. Furthermore, details in the submicroscopic structures of these natural labels offer tantalizing clues to how living organisms were genealogically linked through bygone ancestors. Thus, lengthy DNA sequences housed in the cells of all organisms carry not only the necessary molecular genetic instructions for life, but also extensive records of phylogeny, i.e. of evolutionary ancestry and descent.

During the replication and transmission of DNA from one generation to the next, mutations continually arise. Many of these spread through populations (via natural selection, or sometimes by chance genetic drift), thereby cumulatively altering particular molecular passages in each species' hereditary script. In recent years, scientists have learned how to read and interpret the genealogical content of these evolutionary diaries – these “genomic autobiographies” – of nature. Results are summarized as phylogenetic diagrams that depict how particular forms of extant life are connected to one another via various historical branches in the Tree of Life.

Phylogenetic analysis has become a wildly popular exercise in many areas of biology, but phylogenies estimated from DNA sequences are seldom the ultimate objects of scientific interest. The primary value of each molecular phylogeny lies instead in its utility as historical backdrop for deciphering the evolutionary histories of other kinds of biological traits such as morphologies, physiologies, behaviors, lifestyles, or geographical distributions.

Long before the concept of biological evolution entered the human mind, people classified diverse forms of life into recognizable categories. Some of the earliest spoken words undoubtedly were names ascribed by primitive peoples to particular types of plants and animals important in their daily lives. Theorists and professional biologists categorized organisms too. For example, in the third century BC the Greek philosopher Aristotle grouped species according to morphological conditions (such as winged versus wingless, and two-legged versus four-legged) that he supposed had been constant since the time of Creation. About twenty centuries later, Carolus Linnaeus – a Swedish botanist and the acknowledged father of biological taxonomy – classified organisms into nested groups (such as genera within families within orders within classes), but still he had no inkling that varied depths of evolutionary kinship might underlie these hierarchical resemblances.

More time would pass before scientists finally began to understand that life evolves, and that historical descent from shared ancestors was responsible for many of the morphological similarities among living (and fossil) species. This epiphany is sometimes mistakenly attributed to Charles Darwin (CD), but several scientists before him in the late 1700s and early 1800s, including Jean-Baptiste Lamarck, Comte de Buffon, and CD's own grandfather Erasmus Darwin, were well aware of the reality of evolutionary descent with modification. What CD “merely” added was the elucidation of natural selection as the primary driving agent of adaptive evolution (this achievement was, of course, one of the most influential in the history of science).

Before closing, I want to reiterate two disclaimers. First, although I have emphasized the utility of molecular phylogenies as historical backdrops for interpreting organismal ecology and evolution, this was done primarily to provide a coherent theme and organizational framework for this book. In truth, phylogenies can also be successfully estimated by using all sorts of morphological, behavioral, and other organismal traits. Indeed, all phylogenies erected before the 1960s, and many since then, have been based on directly observable phenotypic traits rather than on proteins and nucleic acids. Usually, well-supported molecular phylogenies tend to agree with seemingly well-supported morphological phylogenies, as expected. Occasionally, however, they appear at face value to disagree; as I have tried to illustrate by examples, resolution of the discord can be mutually illuminating about both molecular and organismal evolution. I have emphasized molecular phylogenetic approaches because they have offered exciting new perspectives on the biological world, and if I disproportionately spotlighted apparent phylogenetic conflicts between different types of data, it is only because these are the most scientifically interesting.

Second, for any or all of the case studies examined, the specific biological conclusions reached (either by the original authors or by myself) remain provisional for several reasons. For example, there is ongoing debate about the relative phylogenetic merits of different types of molecular data and their statistical analyses, controversies continue about precise historical relationships within many if not most of the taxonomic groups considered, and reservations typically abound about numerous details of the comparative phylogenetic approach and PCM analyses themselves (see Chapter 1 and the Appendix).

For creatures that emit or receive visual cues, body colors (or lack thereof) often serve key communication roles. In the context of predation, for example, conspicuousness in the form of blatant warning colorations can be a key to individual survival for both toxic prey organisms and their potential predators, whereas crypsis usually benefits prey that are highly palatable. In the context of sexual communication also, body colorations can influence genetic fitness through their rather direct impacts on reproductive success. Brightly colored males, for example, may tend to acquire more mates than their drab competitors, and hence be evolutionarily favored by sexual selection (see several sections below).

Colors are sensations of light induced in the nervous system of beholders by electromagnetic waves of various frequencies. In terms of biological effects, colors can be thought of as functional outcomes of mechanistic interactions between a transmitter and a recipient, so different observers may perceive the same object differently (for example, many pollinating birds and insects are highly attuned to ultraviolet flower colors that are invisible to people and most other mammals). However, colors also can be interpreted as the electromagnetic wavelengths themselves, in which case they become properties of the light source and the transmitting organism's reflective surfaces (irrespective of observer perceptions). In that sense, too, reflected wavelengths per se become another aspect of an organism's external phenotype. Regardless of how they are “viewed,” body colors have been the subject of a sufficient number of PCM analyses to warrant a separate chapter here.

Geography is another “trait” that can be subjected to PCM. In this case, the geographical arrangements of species (i.e. their character states with respect to space) are plotted onto species' phylogenies as estimated from molecular or other genetic data. The usual intent is to reciprocally illuminate the geological histories of landforms (or bodies of water) and the evolutionary histories of organismal lineages that have inhabited those areas. For example, about three million years ago the Isthmus of Panama gradually emerged above sea level, creating a land bridge that facilitated movements of terrestrial organisms between North and South America and effectively blocking genetic interchanges between marine populations in the tropical Atlantic versus Pacific Oceans. The phylogenetic impacts of this geophysical event can be studied today by comparing molecular patterns among living species in that part of the world.

Strictly speaking, geographic features do not evolve (only biological entities do), but they certainly change through time in response to geological and other physical forces of the planet, and they certainly can leave major evolutionary genetic footprints on conspecific populations, closely related species, and broader taxonomic groups. Furthermore, the evolutionary pathways marked by these phylogenetic footprints often lead researchers to new discoveries about cryptic species or otherwise unrecognized biodiversity hotspots that can be highly important in conservation efforts.

Afrotheria theory

For several decades, geologists have known that continents drift about the surface of the planet, sometimes moving apart and sometimes colliding with one another like bumper cars in a circular arena.