Phylogenetic Patterns as Tests of Speciation Models

4 Phylogenetic Patterns as Tests of Speciation Models Peter J. Wagner and Douglas H. Erwin

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Most-paleobiological discussions about phylogeny have focused on particular transitions from an ancestral species to a descendant one, or on a few transitions within a single taxon (e.g., Gingerich 1985). Although valuable, these studies represent individual examples of a pattern of speciation rather than tests of the generality of any particular mode. Moreover, adequately documented speciation events are very rare. Consequently, even if the investigators have a hypothesis about a clade's phylogeny, they usually lack any direct evidence of the evolutionary processes that produced that phylogeny. A different approach to testing hypotheses about patterns of speciation among fossil species involves a strategy of examining phylogenetic patterns. Different speciation models predict different relationships between speciation and the survival of ancestral morphologies. More specific models also postulate different associations between species-level traits (e.g., temporal and geographic ranges) and the likelihoods of leaving de~cendants ..Therefore, several additional predictions stem from the hypothesis that a particular mode of speciation (vicariance, peripheral isolation, etc.) predominates within a clade. These include which patterns of speciation (anagenesis, bifurcation, cladogenesis) and phylogenetic branching (polytomies, pectinate branches, etc.) should be most common, and the relative likelihoods of sampling plesiomorphic and apomorphic species from the fossil record.

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Because hypotheses about modes of speciation ultimately make predictions about the phylogenetic geometries of clades, phylogenetic patterns can be used to corroborate or refute hypotheses predicting that particular modes of speciation were dominant among closely related taxa. Here we will provide examples of the phylogenetic patterns produced bycladogenesis, anagenesis, and bifurcation. Although reticulation certainly is common among plants and possibly more common among animals than generally realized (e.g., Smith 1992), it is much more difficult to recognize in the fossil rec?rd. We therefore will not discuss examples of reticula tion. We will use two previously published computer simulations of phylogeny to highlight how different assumptions about speciation patterns produce very different phylogenetic patterns. We then use some basic assumptions derived from the simulated results to examine two examples from the fossil record. We aJso discuss why cladograms alone are insufficient to describe phylogenetic patterns without hypothesizing about ancestor-descenda,nt relationships and evaluating temporal or geographic data. Finally, we examine why phylogenies must be interpreted without preconceptions about how speciation proceeds and the implications of this for phylogenetic systematics and comparative biology.

Definitions of Terms Because patterns of speciation have been defined differently by various authors, we will define exactly how we are using each term. The original definition of "dadogenesis" (Rensch 1959, p. 97) included two patterns: (1) ancestral lineages giving rise to two daughter lineages, with the ancestral morphology disappearing, and (2) ancestral lineages "branching" into new daughter lineages with no necessary change co-occurring in the ancestral morphology (see figure 4.1). Some modern definitions (e.g., Maddison and Slatkin 1991; Nixon and Wheeler 1992) restrict cladogenesis to the first pattern. Other definitions (e.g., Raup 1977; Raup and Gould 1974) restrict cladogenesis to the second. The definition that restricts cladogenesis to the first pattern incorporates elements of anagenesis (i.e., the replacement of an ancestral morphology by a derived morphology within a single lineage) because it assumes that the ancestral morphology becomes "pseudoextinct." Combining anagenesis and cladogenesis is confusing; therefore we restrict

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our own definition of cladogenesis to the second pattern and use "bifurcation" to describe the first pattern. In addition, although some workers do not consider speciation to occur via anagenetic evolution ("phyletic evolution" versus "speciation," sensu Larson 1989), we will consider bifurcation a pattern of speciation here. Table 4.1 lists some modes of speciation and the patterns of speciation and phylogenetic topologies that they predict. As with patterns of speciation, the definitions of modes of speciation have varied. Our "vicari-

b

a

Figure 4.1 The two patterns encompassed by Rensch's (1959) definition of "cladogenesis." (a) Ancestral species become pseudo-extinct (t) during a bifurcation into two derived daughter lineages. (b) Derived species branch off from ancestral ones, with the ancestral species conserving a nonderived morphology. Here we use cladogenesis to refer to the second pattern only, while we define the first pattern as bifurcation.

Table 4.1 Modes and Patterns of Speciation Mode

Selection-Driven Divergence Sympatry Parapatry Vicariance Anagenesis Peripheral Isolation Hybridization

Speciation Pattern (typical)

Phylogenetic Pattern

Bifurcation Bifurcation Bifurcation Bifurcation Pseudo-extinction Cladogenesis Reticulation

Symmetric Symmetric Symmetric Symmetric Pectinate Polytomy ?

"symmetric" = "balanced" of Heard 1992; "pectinate" = "Hennigian comb" of Panchen 1992 and "unbalanced" of Heard 1992. NOTES: Hypothesized modes of speciation are matched with the typical speciation patterns each predicts and with the phylogenetic pattern expected if that mode predominates within a clade.

SOURCES:

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ance" encompasses both the "type II" and "type III" allopatry of Brooks and McLennan (1991). We use "peripheral isolation" (sensu Mayr 1963 = "peripatry" of Mayr 1982) for Brooks and McLennan's "type I" allopatry. Because definitions of allopatry have encompassed very different patterns of speciation, we do not use that term here.

Effects of a Priori Assumptions of Interpreting Phylogenetic Pattern If we are to use phylogenies to test hypotheses about speciation patterns, then the methods of phylogenetic reconstruction must not assume a particular speciation model. Many workers appear to think that cladistic (parsimony) analyses require a bifurcating pattern of speciation (e.g., Lorenzen and Sieg 1991). This is not entirely correct. For example,the matrix shown in figure 4.2 yields a single most parsimonious tree with a polytomy. Nevertheless, many phylogenetic systematists do assume that bifurcation is the standard pattern of speciation (e.g., Hennig 1966; Maddison 1989; Slowinski and Guyer 1989a,b; Nixon and Wheeler 1992; Heard 1992) when interpreting cladograms. Such systematists would not interpret the polytomy in figure 4.2 as one species giving rise to four but as an artifact of ignorance. The assumption (often explicit) is that most, if not all, polytomies are the result of inadequate data, and that inclusion of more characters would "resolve" some bifurcating pattern. The assumption of bifurcation obviously imposes a particular pattern of speciation on the interpretation of evolutionary patterns and ignores speciation models that allow a single species to produce multiple daughter

Species A B C D E

a Figure 4.2

I 1 1 1 1 1

Characters II III IV 0 0 0 0 1 0 1 1 0 1 1 0 0 1 0

V 0 0 0 0 1

A

B

C

D

E

A data matrix (a) whose most parsimonious solution produces a polytomy, shown in (b). Without other data, it cannot be determined whether this pattern is due to a single species giving rise to several others or to insufficient data. However, this topology should be found by any parsimony algorithm that does not assume bifurcation.

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species. To avoid such assumptions, we will take a cue from recent methodological works in comparative biology (e.g., Harvey and Pagel 1991) and assume that the cladograms presented here are more or less correct even if they illustrate polytomies. We therefore accept some polytomies as signal rather than noise.

Models of Speciation and the Phylogenetic Patterns They Predict Figure 4.3 shows the phylogeny of a bifurcating lineage. Commonly cited mechanisms for bifurcation include selection-driven divergence (e.g., Darwin 1859; Gingerich 1976), sympatry (e.g., Maynard Smith 1966; Wake, Yanev, and Frelow 1989), parapatry (e.g., Lande 1982), and vicariance (e.g., Lynch 1989; Brooks and McLennan 1991). Although it has been noted that a descendant lineage could retain a plesiomorphic morphology (Nixon and Wheeler 1992), this is not the prediction of selection-driven divergence nor is it a likely prediction of vicariance (e.g., see Brooks and McLennan 1991). Slowinski and Guyer (1989a,b; see also Guyer and Slowinski 1991) used three algorithms to generate cladograms, one of which generated phylogenies using only bifurcation. These simulations assumed that all species were equally likely to leave descendants, so extrinsic features such as temporal and geographic raJlges were not relevant to the outcomes. Also, the possibility of true extinction was ignored. If all species are assumed to be extant and only bifurcation occurred, only three evolutionary trees are possible (figure 4.4a-c). Each of these possible trees can be depicted as a cladogram (d from a, e from b, f from c). These cladograms each assume that the ancestral species became "pseudoextinct" after each speciation event. If, however, these assumptions are relaxed and fossil taxa and polychotomies are allowed, then the addition of ancestral species produces very different cladistic patterns for the same original trees (cladograms g-i). If one predicts (or merely assumes) that bifurcating patterns of speciation predominated within a clade, then one also is hypothesizing that the apparent extinction of plesiomorphic species should be statistically indistinguishable from the apparent originations of daughter lineages. (For discussions on statistical tests of the apparent origins and extinctions of fossil species, see Marshall 1990 and this volume.) Bifurcation models also predict that two derived sister species should share statistically in-

II

I_I

Figure 4.3

A bifurcating phylogenetic pattern. Although this pattern sometimes is terme4 "cladogenesis," the pattern shown here is equally anagenetic, as ancestral morphologies are replaced by descendant morphologies. Therefore, we have reserved the term cladogenesis for a different phylogenetic pattern. In this and in all following figures, ancestral species are given in gray whereas those without descendants are given in black.

Figure 4.4

Three possible phylogenies (a-c) for five species if bifurcation is the only mode of speciation. Note that we assume no extinction and complete sampling of the taxon. "t" denotes the pseudo-extinction of the ancestral lineage at each bifurcation. (d-f) Three cladograms for the final five species produced in Slowinski's and Guyer's (1989) simulations. These simulate sampling species from one time line (e.g., the present), given the assumption that ancestral morphologies cannot be sampled. (g-j) The previous three cladograms with ancestral species included.

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~l-l '"

--1

a Figure 4.5 Phylogeny of anagenetic change (a) with corresponding cladograrn (b). Although each "species" is represented by a vertical band in (a), this is meant solely to represent the temporal range of a morphotype, not to imply morphologic

stasis ..

distinguishable first appearances in the fossil record. Although some workers have considered the latter statement to be true of all sister taxa (e.g., Cracraft 1981), it is necessarily true only for cases in which speciation actually followed a bifurcating pattern. Figure 4.Sa depicts a lineage in which only anagenesis occurs. A cladogram of "morpho species" from this lineage should be completely pectinate (sensu Slowinski and Guyer 1989a,b; = "unbalanced" of Heard 1992) and all of the lineages save for one would be plesiomorphic (figure 4.Sb). Both gradual and punctuated models can predict anagenetic speciation (Wright 1931, 1932; see Jablonski 1986, Provine 1989, and MacLeod 1991). Boucot (1978) has argued that this is indeed the dominant pattern observed in the fossil record. Predictions that anagenetic modes of speciation predominated within a clade thus posit that plesiomorphic species should be fairly common and that the temporal ranges of those species should cease where the ranges of (relatively) apomorphic species begin. One might also predict general congruence between the geographic ranges of plesiomorphic and apomorphic species. Speciation models that predict cladogenesis include models of peripheral isolation (e.g., Mayr 1963; Eldredge 1971; Eldredge and Gould 1972) and some interpretations of the shifting balance theory (e.g., Wright 1982; Eldredge, this volume). These models do not predict that the evolution of . a daughter species necessarily coincides with the extinction of the ancestral species. Furthermore, because the factors affecting speciation and resistance to extioction in some models (i.e., the number of demes and their spatiotemporal distributions) are not necessarily altered by speciation (e.g., Wright- 1982; Lande 1980, 1986), these models may even predict that the ancestral lineage is more likely to speciate in the future than is the descendant one.

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,.,w W

u

V

J

J J

J

-~~~~~~~~~~~~~~~~~~~~~~~~~~~ Figure 4.6

A segment of the "triloboid" phylogeny taken from the MBL simulations and stereotyping cladogenetic evolution as defined in this chapter.

As already noted, we use "bifurcation" to distinguish one of the two patterns of speciation included within the term "cladogenesis" that is used (too broadly, in our view) by some systematists. Although Maddison (1989) referred to "multiple speciation," where one species gives rise to several descendants, he discussed it as an event (i.e., trifurcation, quadrifurcation, etc.) and thus a special case of processes that produce bifurcation (e.g., "type III" allopatry of Brooks and McLennan 1991). Nixon and Wheeler (1992) acknowledged that one daughter lineage can be indistinguishable from the ancestral morphology, which leaves a pattern indistinguishable from our definition of cladogenesis. However, they did not discuss the possibility or likelihood of the plesiomorphic lineage pro. ducing additional daughter taxa.

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The well-known MBL phylogeny simulation (e.g., Raup and Gould 1974; Raup 1977) used cladogenesis (as we narrowly define it) exclusively as the pattern of speciation. Because probabilities of extinction and speciation were held constant, the past history of a lineage (i.e., age ornumber of daughter lineages) did not affect its immediate prospects. Figure 4.6 shows a segment of this phylogeny, and figure 4.7a gives the corresponding cladogram. Figure 4.7b-e depicts cladograms for other segments of the "triloboid" phylogeny. An abundance of polytomies reflecting the actual relationships among "triloboid" species clearly predominates. In addition, a strong association exists between the temporal range of aspecies and the number of descendants it leaves. If modes of speciation conducive to our restricted definition of cladogenesis predominate within a clade, then an association between the extinction of one species and the appearance of another is not necessarily expected. Based on the MBL simulation, we might expect a positive association between plesiomorphic species and either longer temporal

c

e

Figure 4.7 Cladogram accompanying figure 4.6; b-e cladograms reflect larger segments of the triloboid phylogeny than does a. Derived from Raup 1977.

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ranges or whatever factors are conducive to longer temporal durations. Finally, we actually expect polytomies and some "sister taxa" with different times of origin.

Why Cladistic Topology Is Insufficient for Discerning Patterns of Speciation . Although cladograms are often referred to as "phylogenies,"