Origins 52:7-27 (2001).
WHAT THIS ARTICLE IS ABOUT
The subtribe Flaveriinae (Asteraceae: Helenieae) includes a number of plant species sometimes called yellowtops, glowworts, and false broomweed. Different species of this subtribe differ in their chemical pathways involved in photosynthesis. Some species use a system known as C3 photosynthesis, some use a system known as C4 photosynthesis, and others display characteristics intermediate between the two. The authors apply a creationist research method known as baraminology to determine whether the species might have been created separately, or whether they may have descended from a single created ancestral species. They present a large amount of evidence that suggests the entire subtribe belongs to a single lineage which includes additional species not included in the study. The evidence also implies that the originally created ancestor used C3 photosynthesis, and that the C4 photosynthesis present in some species emerged since the creation. The characteristics of the intermediate species and the genetics of C4 species support the hypothesis that latent genetic information may have been present in the ancestor, and activated during post-Flood diversification of the group, possibly through a mechanism called Altruistic Genetic Elements.
Creationists have long speculated whether the
"created kind" can be approximated by a traditional Linnean
classification level (Marsh 1976), with several creationists proposing that
kinds may be equivalent to families (Jones 1972, Siegler 1978, Woodmorappe
1996). In general, these speculations are based largely on hybridization studies
of vertebrates or on the lists of organisms in Leviticus. Although the
family/kind approximation may be adequate for mammals and birds, for many other
types of organisms this estimation may certainly be incorrect. Flowering plant
families frequently contain thousands of species. For example, the Iridaceae
contains 1500 species, the Melastomataceae 4000 species, and the Euphorbiacea
7500 species (Cronquist 1981). The largest plant family is Asteraceae, with
estimates ranging from 20,000 species in 1100 genera (Cronquist 1981) to 30,000
species in 2500 genera (Kim and Jansen 1995). While it is certainly possible
that the Asteraceae could be a single created kind, its species diversity would
be without parallel among the vertebrates. Thus, the magnitude of variation in
the plants should be cause for skepticism in too quickly equating
"family" with "created kind."
As a preliminary case study of created kinds in plants, we present here a review of the taxonomy and phylogeny of the plants of subtribe Flaveriinae (Asteraceae). Wise's (1992) method of baraminology evaluates additive and subtractive evidence separately in an attempt to approximate the complete membership of the created kind, or holobaramin. Additive evidence suggests that two species are genealogically related and is used to delineate monobaramins. Properly understood, monobaramins are simply a group of species which share a common ancestor; the group may be monophyletic or paraphyletic. By revealing a common developmental mode, the traditional hybridization criterion (Marsh 1976) is a source of additive evidence. Subtractive evidence suggests that two species or groups have a separate ancestry and is used to define apobaramins. An apobaramin is any group of species that are separated from all other species by a phylogenetic discontinuity; the apobaramin may contain one or more holobaramins. Novel biological features, such as flight in bats, are frequently used as subtractive evidences. Additive and subtractive evidence can also be evaluated together using the ANalysis Of PAttern (ANOPA) method, which is effective in identifying significant continuity and discontinuity in phylogenetic data (Cavanaugh and Sternberg, in prep).
Currently, two different definitions of subtribe Flaveriinae exist. Flaveriinae sensu stricto includes only three genera, Sartwellia (4 spp., Turner 1971), HaploŽsthes (3 spp., Turner 1975), and Flaveria (21 spp., Powell 1978); while Flaveriinae sensu lato includes those three genera and the genera Clappia, Jaumea, Pseudoclappia, and Varilla (Karis and Ryding 1994). For simplicity's sake, herein we will use the strict definition of Flaveriinae with only three genera, referring to Flaveriinae sensu lato where necessary.
The plants of each genus of Flaveriinae prefer gypsiferous soils in arid climates. Sartwellia and HaploŽsthes are both found in overlapping ranges in New Mexico, Texas, and Mexico (Turner 1971, 1975). The range of Flaveria extends from the southwestern United States through Central America into South America and includes Florida and several Caribbean islands. Isolated Flaveria species are also found in Africa, India, and Australia (Bremer 1994, Powell 1978). Like all Asteraceae, the Flaveriinae reproduce by miniature flowers, which are aggregated into heads resembling larger single flowers, and one-seeded achenes (such as the familiar, striped shells containing the edible sunflower seeds). Unlike other Asteraceae, Flaveriinae contain large amounts of sulfated flavonoids, presumably as an adaptation to or consequence of the saline, sulfate-rich niches they occupy (Powell 1978).
The genus Flaveria is surprisingly diverse, containing annual and perennial species as well as woody and herbaceous species. Most remarkable of all, Flaveria is one of only a handful of genera that contain species that photosynthesize by the C3 and C4 pathways as well as various C3-C4 intermediates.
To review, the C3 plants fix carbon dioxide into a three-carbon compound, 3-phosphoglycerate (3-PGA). This reaction is catalyzed by the enzyme ribulose 1,5-bisphosphate carboxylase/oxygenase (rubisco). 3-PGA then proceeds through a series of reactions known as the Calvin cycle, whereby CO2 from the atmosphere is incorporated into sugars. True C4 plants are characterized by the presence of Kranz anatomy, a ring of specialized bundle sheath cells (BSC) that surround the veins of the leaf. CO2 is fixed in the regular mesophyll cells (MC) of the leaf into a four-carbon compound, oxaloacetate or malate, catalyzed by phosphoenolpyruvate carboxylase (PEPC). These four-carbon compounds ultimately are transported to the BSC where they are broken down, releasing carbon dioxide, which is then fixed into 3-PGA by the enzyme rubisco (Figure 1). The advantages of C4 photosynthesis include better nitrogen-use efficiency and lower photorespiration than in C3 plants (Edwards and Walker 1983).
Although it may seem that this difference in biochemistry is sufficient to warrant the inference of direct divine design, the evidence is far from conclusive. There is no single C4 pathway; to date, three different subgroups have been described based primarily on the different enzymes used to liberate the CO2 from the four-carbon compounds transported to the BSC. The different subgroups use PEP carboxykinase, NADP-malic enzyme, and NAD-malic enzyme to catalyze this reaction. Furthermore, 23 different species in seven different genera and five different families have been identified as exhibiting traits intermediate between C3 and C4 photosynthesis (Monson and Moore 1989). These intermediate traits can be limited to simple anatomical changes in the cells surrounding the BSC, or may include biochemical alterations such as compartmentation of enzymes into the rudimentary BSC. All C3-C4 species possess a limited Kranz-like anatomy of specialized BSC that lack the thickened cell walls characteristic of true C4 BSC (Monson et al. 1984). Many of the BSC of C3-C4 species also concentrate organelles (mitochondria, chloroplasts, and peroxisomes) that contain enzymes critical to the C4 pathway. In Flaveria, a limited C4 pathway and enzymatic compartmentation has been observed in F. ramosissima (Monson et al. 1984). C3-C4 intermediates typically undergo photorespiration less than C3 species but more than C4 (Moore et al. 1987).
Figure 1. A simplified C4 photosynthesis pathway of the NADP-ME type, as found in Flaveria species. CO2 is fixed in the mesophyll cells by phosphoenolpyruvate (PEP) carboxylase yielding oxaloacetate (OAA). The OAA is converted to malate and then transferred to the bundle sheath cells (BSCs). The CO2 is released in the BSC by NAD malic enzyme yielding pyruvate. The CO2 is then fixed by rubisco yielding 3-PGA, which is delivered to the Calvin cycle for normal photosynthesis. The pyruvate is returned to the mesophyll for recycling into PEP. Note that in C3 plants, the pyruvate cycling pathway does not exist. Only the reactions highlighted in grey occur in all leaf cells in C3 plants. (Figure after Edwards and Walker 1983)
baraminology matrix (1992) consists of a series of questions designed to allow
researchers to detect phylogenetic discontinuity. Unfortunately, many of the
questions in the matrix do not apply to the Flaveriinae. For instance, there is
no mention of the Flaveriinae in the Scripture, nor could we find any reference
to fossil Flaveriinae. Though the matrix cannot be used, the traditional
baraminological practice of examining additive and subtractive evidence will be
presented (Wise 1992, Robinson 1997, Robinson and Cavanaugh 1998a, Robinson and
Cavanaugh 1998b ).
Additive Evidence. Hybridization between the members of Flaveriinae is extensive. In the wild, only F. floridana and F. linearis readily hybridize (Monson 1989). The remainder of the crosses summarized in Figure 2 are the result of artificial hybridization studies conducted by Powell (1978). These hybrids are very good evidence for the assignment of monobaramin status to each of the Flaveriinae genera. Of 59 Flaveria interspecific crosses reported by Powell, 40 were successful (Figure 2). Of the six possible interspecific crosses within Sartwellia, two were observed to be successful, and the two HaploŽthes species were also successfully crossed. These crosses are strong indicators of the monobaraminic status of each genus of Flaveriinae.
Hybridization within genus Flaveria reveals a significant pattern of hybridization success versus photosynthesis type (Figure 3). At the time of Powell's experiments in the 1970s, no C3-C4 intermediates had been conclusively identified, although they were suspected to exist. Nevertheless, examination of the hybridization data reported by Powell indicates a clear hybridization success bias between the different photosynthesis types. No cross between a C3 and C4 species was directly successful, indicating that perhaps the different photosynthesis types may themselves constitute monobaramins. The monobaramin status of genus Flaveria is not necessarily called into question by this data, if one assumes associative hybridization in baraminic assignments (Scherer 1993). For instance, F. pringlei (C3) crosses with F. oppositifolia (C3-C4) which crosses with F. linearis (C3-C4) which crosses with F. palmeri (C4). Thus, gene flow between C3 and C4 species can be achieved.
Figure 2. Known hybrids from subtribe Flaveriinae. Black squares represent known successful hybrids as described by Powell (1978). The diagonal line separates the male parent on the left from the female parent on the right. Artificial crosses of Flaveriinae species were conducted in a greenhouse. Crossability was determined by visually estimating seed-set, as described by Powell (1972). Fertility of the F1 hybrids was not reported.
Powell also attempted more than 30 intergeneric crosses, but only four were successful. Significantly, these four intergenerics unite the species of all three genera, including the Flaveria outlier from Grand Canyon, F. mcdougallii, which hybridizes with no other Flaveria species. Again, by assuming associative hybridization, gene flow can be achieved between any species of Flaveria and F. mcdougallii via crosses with Sartwellia puberula (Figure 2). The sterile F1 intergenerics were described as "intermediate in morphology between the grossly different species involved" (Powell 1978). The success of the intergeneric crosses argues for the assignment of monobaramin status to the entire Flaveriinae subtribe, and the morphologically intermediate condition of these plants further supports this assignment (Wise 1992).
Figure 3. Successful hybridizations (represented by the dark lines connecting species names) between the photosynthetic types in Flaveria (based on data from Powell 1978). Connecting lines indicate successful hybridization. See Figure 2 for explanation of hybrid success.
Subtractive Evidence. Unfortunately, subtractive evidence in the literature regarding subtribe Flaveriinae is scarce. No artificial hybridizations between a Flaveriinae species and a member of a separate subtribe have been reported; thus, the failure of hybridization gives no insights into reproductive isolation of the subtribe. Although the Flaveriinae possess 18 chromosomes universally, the predominant chromosome number for the tribe Helenieae is n=19, with other members of Flaveriinae sensu lato possessing 16 or 19 chromosomes (Lundberg 1996). The difference may be due to simple Robertsonian rearrangements, and in light of chromosomal rearrangements in mammals (Gibson 1984, 1986) and Arabidopsis chromosomes (Lin et al. 1999), it is unlikely that chromosome number will ever be a strong subtractive evidence. A phylogenetic analysis of Flaveriinae sensu lato has been conducted by Lundberg (1996). He found 12 equally parsimonious trees, all of which show a consistent clustering of the three genera Flaveria, Sartwellia, and HaploŽsthes apart from the other genera of Flaveriinae sensu lato. From the perspective of additive evidence, this is good reason to assign Flaveriinae the status of monobaramin, but Lundberg's dataset provides very poor subtractive evidence (see below).
Figure 4. Hybridization and DNA similarity in the genus Flaveria. Successful hybrids are shown in black. Species within the DNA similarity range of the hybridizing species are shown hatched.
The baraminological interpretation of the ANOPA results is far from clear. Whereas the additive evidence strongly supports the monobaraminic status of Flaveriinae, the ANOPA results do not support apobaraminic status of the same group of species. This would suggest that Flaveriinae is probably a member of a larger holobaramin that includes at least the species of Flaveriinae sensu lato, and probably the species of Pectidinae as well. This would be consistent with the ndhF phylogeny that showed a close relationship between F. ramosissima and T. erecta. Unfortunately, the ANOPA results show no significant gaps between any of the species tested, thus it is not possible to establish the boundary of the apobaramin of which Flaveriinae is a part.
Figure 5. 1D ANOPA results for Flaveriinae and Pectidinae from the morphological data of Lundberg (1996). Outgroup species of Pectidinae are indicated with horizontal arrows. See results for explanation of axes.
Figure 6. 2D ANOPA results for Flaveriinae and Pectidinae from the morphological data of Lundberg (1996). Species indicated are as follows: Dyssodia paposa (Pectidinae, Dpapo), Tagetes micrantha (Pectidinae, Tmicr), Tagetes lucida (Pectidinae, Tluci), Chrystactinia mexicana (Pectidinae, Cmexi), HaploŽsthes greggi (Flaveriinae, Hgreg), Sartwellia puberula (Flaveriinae, Spube), and Jaumea carnosa (Flaveriinae sensu lato, Jcarn). See results for explanation of axes.
We initiated this study to address two
questions: First, can the holobaramin be approximated as the family for
nonvertebrates? Second, have C3, C4, and C3-C4
plant species descended from a common ancestor, thus implying the post-Creation
emergence of biological complexity?
From our present analysis, we were unable to answer the first question definitively. We could not define any clear apobaraminic unit to which Flaveriinae belongs, allowing for the possibility that the entire family Asteraceae is a holobaramin. One observation in favor of this interpretation is the fossil record of the family Asteraceae. The family does not appear in the fossil record until the Oligocene and diversifies substantially by the Miocene (Bremer 1994, DeVore 2000). This Cenozoic appearance and diversification is similar to other post-Flood vertebrate baramins (Wise 1994, Wise 1995, Garner 1998, Wise 1999).
The second question regarding the origin of C4 photosynthesis has been answered quite clearly. All of our evidence supports the view that all species of the Flaveria genus are members of a single monobaramin and therefore share a common ancestor. Since C3 photosynthesis is the predominant type of photosynthesis for species of Flaveriinae and Flaveriinae sensu lato (Lundberg 1996), the most parsimonious interpretation is that the C4 species have developed from C3 ancestors. Based on this conclusion, the C4 photosynthetic pathway is a biochemical pathway that has emerged in Flaveria after Creation and quite possibly post-Flood (considering the fossil record of the Asteraceae mentioned above).
Although the sequence data are insufficient to aid in identifying the apobaramin to which the Flaveriinae belong, the sequences can assist in understanding the monobaraminic divisions within Flaveria itself and the evolution of Flaveria species. A phylogeny of the genus Flaveria rooted by a homologous sequence from Pisum sativum (the garden pea) is shown in Figure 7. The phylogeny shows three distinct groups of Flaveria sequences, corresponding to the C4, C3, and C3-C4 species groups. The phylogeny also shows that the C3-C4 group branches between the C3 and C4 groups, and this may be explained by one of two hypotheses. First, the occurrence of C4 and C3-C4 intermediates group on two different branches implies that the modern C3-C4 species are not true evolutionary intermediates between the modern C3 and C4 species but that extant C3-C4 intermediates are the living descendants of a true evolutionary intermediate population. Alternatively, one may also conclude that C4-like adaptations have arisen twice in the Flaveria, one producing the complete C4 syndrome and one producing only a partial C4 syndrome. To distinguish these explanations, we turn to the geography of the new world species of Flaveria. The distribution of the three photosynthetic types of Flaveria supports the hypothesis that the C3-C4 species are the descendents of the true evolutionary intermediates between the C3 and C4 Flaveria species. The C3 Flaveria species and all species of HaploŽsthes and Sartwellia are restriced in range to Mexico and Texas, implying that the geographic origin of monobaramin Flaveriinae is in this region. The C3-C4 species of Flaveria are found in a restricted geographic band north of the C3 species (Figure 8). Further north still, the C4 species appear, from which they can then spread to a much broader range (Figure 8), including South America and the Australian F. australasica. It is likely that the C3-C4 intermediates are occupying a limited range because of their physiology, while the C4 plants are able to spread out much more readily because of their decreased photorespiration. Thus, when interpreted together, the molecular, morphological, biochemical, and geographic data all point to the evolutionary intermediacy of the ancestors of the modern C3-C4 species.
Because the modern C4 Flaveria species descended from ancestral species that were C3, the C4 photosynthetic pathway must have arisen after the creation of this holobaramin. Thus, one explanation for the origin of C4 photosynthesis can be eliminated: direct creation by God. Superficially, the conclusion that C4 photosynthesis has arisen since creation seems to deny the basic creationist belief that no increase in biological complexity has occurred, that all evolution has been degenerative (Nelson 1967, Morris 1974, Williams 1976, Davis and Kenyon 1993, Sarfati 1997, Sarfati 1999). Eliminating direct creation does not, however, leave gradualistic, accidental evolution as the only alternative explanation. The emergence of C4 photosynthesis fits well with Wise's notion of diversification, a period of rapid speciation immediately following the Flood, which resulted in drastic changes within many holobaramins (Wise 1994, 1996). Recently, Wood has proposed a genetic model called the AGEing process that is capable of explaining numerous features of rapid post-Flood diversification (Wood, in prep). According to this model, intrabaraminic diversification occurs as a result of specially designed mobile DNA sequences called Altruistic Genetic Elements (AGEs). Hypothetically, AGEs are capable of activating or inactivating genetic potential already present in an organism's genome (Wood, in prep). Thus, C4 photosynthesis could be designed without being directly created in its complete form. God could have made the genes necessary for C4 photosynthesis in a latent state and allowed them to become activated at a later date by AGEs. The AGE-induced activation of latent genetic material explains the origin of C4 photosynthesis better than evolution for the following reasons:
Figure 7. Fitch-Margoliash phylogeny of gcsH sequences from Flaveria and Pisum.
Figure 8. Geographic distribution of new world Flaveria species (Data obtained from Powell 1978).
If AGEing is indeed responsible for the
expression of latent C4-specific genetic material in Flaveria,
the various C3-C4 intermediates would represent species
that have not yet had the full suite of C4 genes activated.
Considering the potential for three apparently discrete levels of C4-like
plants (anatomically C4, biochemically intermediate, and completely C4),
this would imply a minimum of three different genetic changes necessary for the
C4 trait to be fully expressed. Support for this theory is found in
the genetics of C4 photosynthesis (Sheen 1999). In particular, C4-specific
genes are known to occur in C3 species of Flaveria (Lipka et
al. 1994). The primary differences between C4-specific genes in C3
and C4 plants is the promoter region which controls the expression of
the gene (Sheen 1999). Further research into the physiology of C4
plants will no doubt shed new light on the source of these promoter differences
in C3 and C4 species.
Regardless of mechanistic explanations, the presence of two very different kinds of photosynthesis in the same holobaramin highlights the elegant design that is so prevalent in the living world. Not only did God create organisms with what they needed at that time; He also provided an abundance of characteristics, which may or may not be immediately apparent, that would be necessary for survival in a world damaged by sin and ravaged by a worldwide Flood. From our narrow, utilitarian viewpoint, we may label a structure 'vestigial' or a strand of DNA 'junk,' but given the proper circumstances, these useless features may prove their value after all. The notion of AGE-activated latent genetic material could become a powerful explanation of apparently useless features of living organisms as simply the unexpressed abundance of a benevolent Creator.
A very early draft of this paper was presented at a meeting of the Baraminology Study Group held at Bryan College, June 27, 1997. We thank Ashley Robinson, Kurt Wise, and our anonymous reviewers for their critical reading of various drafts of this work. Many thanks to Stephanie Mace for assistance in preparing Figure 8.
ANOPA. The cladistic data matrix of
Lundberg (1996) was used for ANOPA analysis. Because ANOPA requires all data to
be coded numerically, unknown character states were recoded as 0's
with subsequent states increased by 1. Thus, a character state in Lundberg coded
as ?, 0, and 1 is here recoded as 0, 1, and 2, respectively. A complete matrix of
the transformed data is available from the authors on request. ANOPA was
performed using standard methodology as described by Cavanaugh and Sternberg (in
Molecular Phylogenetics. The sequence phylogeny was constructed from gcsH sequences obtained from GenBank (http://www.ncbi.nlm.nih.gov) for the following species: F. anomala (Z37524), F. bidentis (Z37517), F. chloraefolia (Z37520), F. cronquistii sequence A from Kopriva et al. (1996) (Z25854), F. floridana (Z37528), F. linearis (Z37521), F. palmeri (Z37529), F. pringlei sequence A from Kopriva et al (1996) (Z25855), F. pubescens (Z37530), F. trinervia (Z37523), and Pisum sativum (J05164). We omitted loci B and C from the C3 plants for simplicity and because the source of the F. pringlei gcsHB is questionable (see discussion in Kopriva et al. 1996). Sequences were aligned with CLUSTAL W v. 1.75 (Thompson et al. 1994) using default parameters. After trimming end-gaps, the final alignment consisted of 359 positions. Distances were inferred using the DNADIST program of the PHYLIP package (Felsenstein 1993). The phylogeny was constructed using the Fitch-Margoliash method (Fitch and Margoliash 1967) as implemented in the FITCH program of the PHYLIP package.
*Corresponding Author, Assistant Professor,
Center for Origins Research and Education, P.O. Box 7731, Bryan College, Dayton,
TN 37321; email@example.com
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