Knaus, Cronn and Liston 1
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Knaus et al.
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A fistful of Astragalus
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A fistful of Astragalus: the morphometric architecture of an infra-specific group.1
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Brian J. Knaus2, 4
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Rich Cronn3
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Aaron Liston2
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Knaus, Cronn and Liston 2
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Manuscript received _______; revision accepted _______.
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Department of Botany and Plant Pathaology, Oregon State University, Corvallis, OR 97331
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USA.
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OR 97331 USA.
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Pacific Northwest Research Station, USDA Forest Service, 3200 SW Jefferson Way, Corvallis,
Author for correspondence (e-mail: knausb@science.oregonstate.edu).
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BJK thanks Richard Halse (OSC) for arranging herbarium loans and support in the herbarium.
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Nancy Mandel and Randy Johnson (USDA FS, PNW) provided help with statistical analyses.
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Peter Dolan (OSU) helped fit sine waves to monthly data. Chris Poklemba (USDA FS, PNW)
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helped with propagation of A. lentiginosus at the Corvallis FSL. Dana York, Kathy Davis, Dell
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Heter, and Patrick and Christine Whitmarsh provided inspiration, locality information, and
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housing during collections. Lisa Graumlich (Montana State University), John King (Lone Pine
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Research, MT), Mark Fishbein (Portland State University), Lucinda McDade (Rancho Santa Ana
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Botanical Garden), Constance Millar and Bob Westfall (USDA FS, PSW) provided inspiration to
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BJK to pursue this study as a graduate program. The title is a tribute to Rupert Barneby who
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titled a series of his papers “Pugillus Astragalorum.”
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Grants!!! NPSO, NNPS, Hardman Award
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ABSTRACT
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The study of infra-taxa has historically been considered the study of incipient species. The
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species Astragalus lentiginosus (Fabaceae) is the most taxonomically complex species in the
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United States flora. The implausible amount of diversity within A. lentiginosus is reflected by its
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taxonomic history. Morphometric data presented here indicate that the varieties lack clear
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regions of distinction, which is congruent with their circumscription as infra-taxa. Significant
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correlations to climatic parameters suggest that the great diversity within A. lentiginosus may be
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due to local adaptation. Existing infra-specific circumscription is surprisingly similar to
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statistical optimization. K-means clustering was employed to determine the number of groups
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but failed to result in an optimal number of groups, suggesting that the varieties are clinal and
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can be divided into an arbitrary number of infra-taxa. The bewildering amount of diversity
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contained within the species Astragalus lentiginosus begs for decomposition yet its clinal nature
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precludes it from division into discrete groups. The use of infra-taxa in this species appears
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useful in that it divides this bewildering diversity, however there does not appear to be an
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optimal method based on morphology to decompose this species. Varieties of A. lentiginosus are
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interpreted as important documentation of infraspecific diversity, however the authors wish to
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stress that these groups should be interpreted as clinal in nature and not discrete.
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Keywords: Astragalus; clines; Fabaceae; Great Basin; Mojave Desert; morphometrics;
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speciation.
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(up to 8)
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INTRODUCTION
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The ‘species’ is considered the fundamental unit of biology (Stebbins, 1950; Mayr and Ashlock,
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1969; Raven and Johnson, 2002; Coyne and Orr, 2004); but see (Bachmann, 1998) Campbell
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and Reese, 200X. While the PLANTS database of United States plants (USDA, 2006) includes
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33,383 species it also includes 3,853 taxa at infraspecific ranks (table 1), indicating that around
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11% of the species in the United States flora include infra-specifics (taxa recognized at the ranks
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of subspecies or variety). If the species is the fundamental unit of biology then of what value is
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the infra-specific rank and why do we have so many of them?
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A unifying theme among species concepts is that the species is somehow ‘discrete’ (Mayden,
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1997; Coyne and Orr, 2004) even though the metric is debatable (e.g., significant morphological
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distinctiveness, reproductive isolation, reciprocal monophyly, etc.). For example, the Biological
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Species Concept (Mayr and Ashlock, 1969) indicates that a species is a group of entities that are
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reproductively isolated from other ‘species.’ This is philosophically attractive because it implies
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that these entities (the species) no longer share a common evolutionary path due to an inability to
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share genetic material. However, theory indicates that adaptive divergence, another important
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concept in evolutionary biology, can occur in spite of gene flow (Wu, 2001; Via, 2002). This
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indicates that ‘groups’ of organisms can diverge to occupy different adaptive peaks while
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reproductive barriers may be incomplete or nonexistent. Therefore an important ‘unit’ of
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evolution may not necessarily require reproductive isolation. However, as long as the transfer of
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genetic material is possible, there is the possibility of intermediates which may represent poorly
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adapted individuals or individuals that are adapted to selective forces that are intermediate to the
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ends of the spectrum. We believe Infra-taxa may represent these entities which represent
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intermediates along a continuum that is too great to be considered as one.
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If a species this is discrete than how does one delineate infraspecies, which therefore must be
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somehow non-discrete? Here we employ the most taxonomically complicated species in the
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United States Flora, Astragalus lentiginosus Dougl. ex Hook. (Fabaceae; USDA, NRCS 2007,
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table 1), to explore the value and delineation of infraspecies.
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A Brief History of Infra-Taxa— Linnaeus is credited with providing the modern system
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of binomenal nomenclature however he also employed the trinomial at the rank of ‘variety’
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(Linnaeus, 1753). Linnaeus considered the species to be the product of creation while the variety
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to be variation that has arisen since the creation (Stearn, 1957). Modern nomenclature has
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adapted an evolutionary system, however, the systems share the concept that infraspecies are
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recently derived.
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One path to speciation described by Darwin (Darwin, 1859) is the increase in variation to a point
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where the magnitude of variation is no longer maintainable, resulting in divergence that ends in
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distinct species. Subsequently he relied on the multitude of artificial selection experiments
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performed informally by breeders (Darwin, 18??; animals under domestication) to demonstrate
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this increase in variation, and how this variation can accumulate in a relatively short amount of
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time. These ideas were somewhat formalized by Fisher (Fisher, 1958) who described the idea of
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‘steady states’ and their maintenance, which would break down at large magnitudes.
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A slightly different perspective was presented by Huxley (Huxley, 1938, 1939) through the study
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of clines. Huxley addressed the study of large amounts of discontinuous variation and sought to
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classify it. Huxley tried to decompose the problem of clines, in part, by proposing the idea of
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stepped clines, clines in which different groups possess a shallower slope than the entire group.
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This usually requires the a priori determination of groups, a move that is as contentious as the
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argument between lumpers and splitters.
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Wilson and Brown (Wilson and Brown, 1953) criticized the subspecific rank. Among their
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points were that the naming of these groups detracted attention from the species and implied a
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discrete nature to these infraspecific groups. This is misleading because it is the ‘species’ that is
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supposedly discrete. This leaves the subspecies as a group of entities whose divisions appear
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arbitrary and therefore may have little value. In a rebuttal to these criticisms Mayr (1953) agreed
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that the infraspecific rank confused the importance of the species (which should be the focus of
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biology) but defended the infraspecies as an important record of infraspecific diversity.
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The controversy surrounding infraspecies continues in the literature. Perhaps the most recent
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critic being Zink (Zink, 2004) who presents mitochondrial data as refuting the evolutionary
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relavence of the infraspecies. A shortcoming of Zink’s argument is that it doesn’t address
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current research topics such as the coalescence (Hudson, 1991; Nordborg, 2001; Hudson and
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Coyne, 2002; Roseberg and Nordborg, 2002) or adaptive divergence (Wu, 2001; Via, 2002;
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Dieckmann et al., 2004). Haig et al. (Haig et al., 2006) have provided a recent review of the
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infraspecies in the context of the Endangered Species Act and biological conservation. They
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supported recognition of the infraspecies in part on grounds that in the United States legal
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protection is applied only to named groups of organisms (particularly in plants) which puts an
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emphasis on recognizing polymorphism, even if it may be geographical.
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What’s wrong with geographical variation???
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Much of the theoretical discussion of the speciation process (Hudson, 1991; Nordborg, 2001;
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Wu, 2001; Roseberg and Nordborg, 2002; Via, 2002; Dieckmann et al., 2004) employs explicitly
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genetic models of evolution. While the discrete character of molecular genetic data (e.g., A, T,
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G or C) promises a discrete answer these authors present theoretical rationale for the existence of
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genetic intermediates. Here we choose to focus on the morphometrics of a varietal complex.
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The phenotype has many obvious relations to the genotype (Falconer and Mackay, 1996; Waitt
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and Levin, 1997; Walsh, 2001) and is of great relevance to the species problem (Rieseberg,
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Wood, and Baack, 2006). The vast majority of plant taxa have been circumscribed based on the
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Linnaean Species Concept, or Morphological Species Concept (Mayden, 1997), based on its ease
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of application and relatively long history. The quantification of the morphological aspects of a
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taxon of evolutionary interest is therefore a logical first step in gaining inference into processes
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that may be active within the group.
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The Most Taxonomically Complex Species in the United States Flora— Astragalus
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lentiginosus Dougl. ex Hook. (Fabaceae) is the most taxonomically complex species in the North
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American Flora (USDA, NRCS, 2007, table 1). The species is distributed throughout the arid
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regions of western North America (Fig. 1) where it frequently occupies disturbed, saline, or
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otherwise marginal habitats. Many of the varieties were originally described as species (Hooker,
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1833; Gray, 1856, 1863; Sheldon, 1894). As collections increased intermediate forms became
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apparent which led to their reduction as varieties (Jones, 1895, 1923). Rydberg (Rydberg,
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1929a, b) employed a very different species concept, elevating the varieties of A. lentiginosus to
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species in the genera Cystium (inflated pods) and Tium (slightly inflated pods). Within the genus
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Cystium he included the subgenera Lentiginosa ,Coulteriana, and Diphysa which were separated
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based on inflorescence length, flower size, and flower color. This grouping is no longer formally
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recognized with a name but is reflected in the modern keys to the group (Barneby, 1964, 1989;
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Spellenberg, 1993; Isely, 1998; Welsh et al., 2003) which largely follow the treatments of
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Barneby. Barneby (Barneby, 1945) returned the group to a single species with numerous
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varieties. Through time several varieties have been reduced to synonymy (Barneby, 1964, 1989)
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while new varieties have also been described (Barneby, 1977; Welsh, 1981; Welsh and Barneby,
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1981; Welsh and Atwood, 2001). As many as 40 varieties have been recognized at once
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(Barneby, 1945; Isely, 1998), currently we recognize 35 (USDA, NRCS, 2007, table 1).
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MATERIALS AND METHODS
Morphometric measurements— Specimens from major western herbaria were measured
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including BRY, JEPS, NESH, NY, ORE, OSC, POM, RENO, RM, RSA, UC and WILLU. A
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goal of 20 specimens, possessing fruit and flower, were attained for the common varieties of A.
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lentiginosus (table 2). Sampling was focused on the widespread varieties for the practical reason
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that these taxa have been most abundantly collected. Some endemic taxa only occur at a few
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localities (e.g., A. l. vars. albifolius, sesquimetralis, and piscinensis). Sampling of endemic taxa,
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even if there were sufficient specimens, would have confounded the sampling of single
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populations versus the range of widespread taxa.
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Fourteen linear morphometric characters were chosen from the keys of Barneby (Barneby, 1945,
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1964, 1989) and measured with a ruler, electronic caliper, or ocular micrometer (table 3). Three
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measurements were made of each structure whenever possible and a mean of these values was
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recorded. Measurements were made from different parts of the plant (e.g., different stems or
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racemes) whenever possible or from different plants when more than one was on a sheet. The
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fourteen characters were: stem internode length, leaf rachis length, leaf petiole length, leaflet
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number, leaflet width, leaflet length, peduncle length, floral axis in fruit, keel length, calyx tooth
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length, calyx tube length, pod length, pod height, pod valve thickness, beak length.
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Assesment of infraspecific structure— All data were examined for univariate normality
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and heteroscedacity using histograms and scatterplots (using the generic functions ‘hist’ and
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‘plot’, R package ‘graphics’)(R Development Core Team, 2007). The characters ‘floral axis in
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fruit’ and ‘pod valve thickness’ were natural log transformed to improve normality. Principle
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components analysis was performed (using the function ‘princomp’ in the R package ‘stats’) on a
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matrix of correlations to explore patterns of structure in the group. Principle components
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analysis is an eigen analysis used to explore data without the a priori assignment of groups
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(Everitt, 2005; Tabachnick and Fidell, 2007). A matrix of correlations was chosen to give each
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character equal weighting in the analysis.
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Assesment of varieties— Discriminant function analysis was performed (using the
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function ‘lda’ in the R package ‘MASS’) to explore structure given the a priori grouping as
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varieties (Barneby, 1964, 1989) both with and without the use of latitude and longitude as
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additional explanatory variables (fig. 3). All characters were standardized by standard deviations
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in order to equalize the magnitude of each character. Discriminant function analysis seeks to
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build multivariate functions that best discriminate among a priori groups (Everitt, 2005;
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Tabachnick and Fidell, 2007). These functions can then be plotted in ordination space.
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In order to asses the optimal number of groups k-means clustering was performed on the data
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(using the function kmeans in the R package ‘stats’). K-means analysis uses a predefined
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number of groups and utilizes an optimality criterion to fit the data within these groups (Everitt,
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2005; Tabachnick and Fidell, 2007). A sum of squares can then be calculated to assess the fit.
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Note that as the number of groups increases the sum of squares is expected to decrease, therefore
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researchers usually examine plots for a breakpoint in the data where additional groups no longer
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appear to dramatically decrease the sum of squares. Standardization by standard deviation was
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performed to equalize the contribution of each trait. In order to explore the sensitivity of the data
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to the optimality criterion several methods were employed (Hartigan-Wong, Lloyd, Forgy, and
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MacQueen).
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Phenological standardization— In order to explore climatic trends in morphology the
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PRISM dataset (Daly et al., 2002) was used. Specimens were assigned a latitude and longitude
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by referencing label information to a place-name database (topozone.com) or converted from
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township and range when available this data was available (www.esg.montana.edu/gl/trs-
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data.html). The spatial join command in ESRI’s ArcView Spatial Analyst (Redlands, California)
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was used to extract elevation, monthly minimum and maximum temperature and monthly
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precipitation from the PRISM dataset.
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Units are sort of mixed up, get radians and days straight
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In order to assign phenologically meaningful data to the monthly PRISM data a sine wave was fit
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to each specimen’s annual set of monthly data using:
y  A sin x  t 
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where y is degrees Celsius, A is [max(temp)-min(temp)]/2 and scales the amplitude of the wave
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(which in radians has a maximum and minimum amplitude of 1 and -1), x is days from January
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1, ω is angular frequency and here is set to 1, and t indicates the initial phase where sin(π/2)=1
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and occurs at 91.25 days. The initial phase was set by averaging the two greatest temperatures
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and subtracting 91.25. Trigonometric functions were performed in radians and were converted
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to days (instead of 360 degrees) with radians = days*π/182.5. The fitting of sine waves was
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performed using the R statistical programming language (R).
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Simple linear regression was performed (using the function ‘lm’ in the R package ‘stats’) using
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morphological characters as well as principle components as dependent variables and climatic
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parameters as independent variables to explore the relative importance of climate on
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morphology. All statistical analyses were performed with R (R Development Core Team, 2007).
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RESULTS
Summarize!!!
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Assesment of infraspecific structure— The naming of infraspecific taxa as well as the
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provision of infraspecific keys implies a discrete nature to these taxa (Wilson & Brown, 1953).
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This hierarchy also implies a high degree of diagnosability to these taxa. Names and keys have
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both been applied to the varieties of Astragalus lentiginosus (Jones, 1923; Barneby, 1945, 1964,
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1989). In order to explore these implications principle component analysis (Fig. 2) and
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discriminant function analysis (Fig. 3) were performed on taxonomically important characters
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(table 3). Principal components analysis (Fig. 2) indicates clustering of morphotypes that show
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cohesiveness to varieties within morpho-space but lack discrete boundaries. Similarily
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discriminant function analysis (Fig. 3a) shows cohesiveness to varieties but no distinctiveness.
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These results demonstrate a clinal nature to the varieties. The varieties appear to occupy
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contiguous ordination space but lack regions of clear distinction. The inclusion of latitude and
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longitude (Fig. 3b) as explanatory variables reveales an increase in structure. This demonstrates
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that a lack of morphometric clustering can be improved by the knowledge of geographic
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position, indicating that the varieties of A. lentiginosus are geographic races. This is intuitive as
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botanists viewing herbarium specimens usually look for label information, and frequently curse
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the collector whom omits locality information.
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Optimal number of groups— In order to asses the optimal number of groups within this
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species, and thus the number of infraspecific taxa, k-means clustering was performed (Fig. 4). It
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is important to note that as the number of groups increases the sum of squares is expected to
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decrease. Researchers are expected to look for a ‘break point’ where inclusion of another group
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does not dramatically decrease the within group sum of squares. There does not appear to be a
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‘natural’ break point in the data (Fig. 4). This indicates that no clear subdivisions exist within
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the excessive amount of diversity contained within this group. The subgenera of Rydberg (1929)
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and the varieties of Barneby (1964) are included for comparison. These data indicate that the
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inclusion of more subgroups decreases the within group sum of squares but does not demonstrate
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a ‘break point’ where the inclusion of another group does not dramatically decrease the within
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group sum of squares. This indicates that there are not any ‘natural’ break points within A.
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lentiginosus. The varieties of A. lentiginosus largely occupy different regions of ordination
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space, but do not occupy discrete regions of ordination space. This is congruent with current
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understanding of infraspecies.
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Climatic correlations— In order to explore climatic correlations principle components
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were compared to climatic parameters. Principle component one is loaded with vegetative
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characters (table 4.) and is highly negatively correlated with dormant season precipitation (Fig.
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5a; R2 = 38.38%, p < 2.2 * 10-16). Principle component two is loaded with floral characters
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(table 4.) and is highly correlated with growing season temperature (Fig. 5b. R2 = 20.9%, p =
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1.082 * 10-10). These statistics imply a significant and dramatic proportion of the variation in
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multivariate diversity to be attributable to climatic factors. While the present study design
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cannot disentangle the relationship between correlation and causation it is nevertheless very
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intriguing that these correlations are so significant and account for a moderate amount of the
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variation in these traits. Meta-analyses (Waitt and Levin, 1997) seem to suggest that the
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correlations may be improved upon if the environmental component of the phenotype is
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controlled for.
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DISCUSSION
Summarize!!!
The importance of the morphological species concept— We have chosen to focus on the
morphological species concept for largely practical reasons, mainly, its ease of application to
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herbarium specimens. Evolutionary biologists frequently refer to the Biological Species Concept
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(Mayr and Ashlock, 1969; Coyne and Orr, 2004) which defines the species as a group of
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organisms that are reproductively isolated from other species. This is philosophically attractive
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because it delimits units which can no longer share an evolutionary fate due to their inability to
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share genetic material. Of the 33,000 species included in the PLANTS database it seems
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doubtful that a large percentage of the taxa have been subjected to tests of interfertility.
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Furthermore, the botanical literature includes numerous examples of interfertility among groups
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which taxonomists have considered to be ‘good’ species (lots of citations). Theory predicts that
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divergence can progress despite gene flow (Wu, 2001; Via, 2002; Beaumont, 2005). Given the
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multiple paths to speciation proposed (Dobzhansky, 1951; Grant, 1981; Coyne and Orr, 2004) it
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seems reasonable to accept a plurality in species concepts (Mayden, 1997). Selection acts on the
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phenotype so here we have chosen to explore phenotypic divergence within A. lentiginosis, a
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process that may exceed that of reproductive divergence (Wilding, Butlin, and Grahame, 2001;
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Beaumont, 2005) (Qst Fst refs).
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Infraspecific structure— The naming of infraspecific taxa and the provision of keys
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implies a discrete nature to infraspecies (Wilson and Brown, 1953). This is in conflict with the
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idea of the species as the fundamental unit of biology, where the ‘species’ is considered discrete.
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Here we’ve demonstrated that the varietal complex Astragalus lentiginosus does not contain
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‘discrete’ varieties. Instead, these taxa occupy cohesive regions of ordination space but lack
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clear or ‘natural’ breaks. The varieties of A. lentiginosus fall along a cline of morphometric
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diversity. This is consistent within the hierarchical system of nomenclature where the
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infraspecies (e.g., subspecies or variety) is subordinate to the species. Within this system the
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‘species’ is considered ‘discrete’ while subdivisions of this category must necessarily be non-
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discrete. This is consistent with the presented data where the varieties of A. lentiginosus are
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contiguous in morphospace but are not discrete.
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Optimal number of groups— The varieties of A. lentiginosus do not fall into coherent
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classes. This is consistent with PCA and DFA not finding discrete groups within A. lentiginosus.
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Instead of falling into easily classified groups the varieties of A. lentiginosus fall into regions of a
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continuum. The morphometric diversity within this group begs distinction, as its taxonomic
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history reflects. However, despite this great morphological diversity, the species A. lentiginosus
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appears to be a cohesive unit, eve if this cohesiveness requires disparate parts of the range in
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order to explain.
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Comparison of Rydberg’s three sections (Rydberg, 1929a) and Barneby’s 14 varieties (Barneby,
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1964) Fig. 4) demonstrates a large coherence between existing taxonomy and the presented
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statistical methodology. While statistical methods do demonstrate an improvement upon existing
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taxonomy it is unclear how dramatic this improvement is. The delimitations of Rydberg
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(Rydberg, 1929a) and Barneby (Barneby, 1964) represent close approximations to the presented
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statistical analysis (Fig. 4.). In the interest of stability in the taxonomic system it seems that any
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‘improvement’ on the system needs to address this lack of discrete boundaries and the
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delimitation of somewhat arbitrary groups.
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The inclusion of several optimality criteria was intended to demonstrate the sensitivity of the
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data to the optimality criterion, however, this does not address the sensitivity of the data to
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differing analysis methodologies. The presented data demonstrate a lack of distinctiveness to the
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varieties, however the varieties do possess
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Climatic correlations— Morphologies of A. lentiginosus have significant correlation to
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climatic parameters (fig. 4) which suggests causation. Climatic change during the beginning of
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the Holocene has been implicated in changing the distributions of plants (Hewitt)(Grayson,
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1993). The distribution of A. lentiginosus includes inland sand dunes, desert seeps, as well as
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regions such as the Lahontan Basin. These habitats have changed dramatically since the last
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glacial maximum and have undoubtedly played a role in the evolution of A. lentiginosus. Here
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we’ve explored the role of climate as a potential selective force that may be responsible for the
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diversity in morphology currently expressed in A. lentiginosus.
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‘Auxiliary’ systems of taxonomy— A vocabulary to describe clinal relationships among
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infrataxa exists as “rassenkreis” (Endler, 1977), clines (Huxley, 1938, 1939) and ecotypes
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(Clausen, Keck, and Hiesey, 1939). This vocabulary does not appear to have become prevalent
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in the taxonomic literature, and hasn’t been mentioned in the literature of A. lentiginosus. This
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may be due to several reasons. Naming implies homogeneity within a group and distinctiveness
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among groups, this perhaps is reflected in the Linnaean background where the ‘species’ is a
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product of Creation. Typification reinforces this idea by suggesting that one specimen is
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representative of an entire taxon. Conversely, there is an insistence from authors such as Mayr
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(1940) who feel that species are inherently polymorphic and that the ‘species’ should be
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considered to contain this diversity. This is perhaps an issue of perspective. Organisms which
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we are unfamiliar with may appear uniform while taxa we are familiar with may appear to host a
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wealth of diversity. The more we study something the more detail we discover. In A.
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lentiginosus we make the argument that while morphological diversity appears to be clinal in
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nature, particularly for taxonomically important characters, this diversity is of a profound range
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warranting division. Furthermore, division facilitates one of the most basic purposes of
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nomenclature and assigns names to allow conversation. The keel lengths of varieties of A.
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lentiginosus range from 7-11 mm, an almost doubling in size. Keel length is not only important
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taxonomically but may be tied to pollinator success, so this may be a character under relatively
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strong selection. It would appear implausible to refer to organisms that are erect, tomentose, and
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purple flowered and prostrate, glabrous, and white flowered by the same name. Therefore we are
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stuck with the issue of applying names to arbitrary divisions along the cline between these two
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extremes.
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The problem of ‘groups’— The major problem within A. lentiginosus is the delimitation
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of groups or statistical ‘factors.’ The ‘species’ may be considered by many to be a ‘natural’
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group. Recent empirical and theoretical research has shown this to be an unreasonable manner to
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group organisms. The geographical ‘population’ has recently been shown to be an untenable
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‘group’ to organize organisms based on migration and admixture (Pritchard, Stephens, and
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Donnelly, 2000; Falush, Stephens, and Pritchard, 2003; Corander and Marttinen, 2006; Falush,
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Stephens, and Pritchard, 2007).
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Conclusion—Astragalus lentiginosus is the most taxon rich species in the U.S. flora.
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Taxa have been historically circumscribed to attempt to account for the amazing amount of
375
morphological diversity contained in the group. We present data which demonstrate
Knaus, Cronn and Liston 18
376
taxonomically important characters to be clinal in nature indicating that the varieties may be
377
arbitrary divisions along this cline. Climatic correlations suggest that the differences within A.
378
lentiginosus may be climatic which are also correlated with geography. We recognize that
379
despite this clinal nature important infraspecific differences are present. These differences have
380
been demonstrated in the quantitative genetics literature and can be demonstrated in the present
381
dataset. Optimization of the varieties could be performed through various methods, such as
382
division of principle components into equal partitions. Molecular data (Knaus in prep) promises
383
to add alternate perspectives on the evolutionary relationships with this perplexing group. Future
384
studies are encouraged to address the issue of clinality when making nomenclatural decisions.
385
Further research into this perplexing group may provide interesting insights into the evolution of
386
morphological complexity, climatic adaptation and diversification.
387
388
A species is an array of populations that are evolving collectively ((Rieseberg and Burke, 2001;
389
Morjan and Rieseberg, 2004). This collectiveness can be facilitated through some level of gene
390
flow, shared retention of ancestral traits, or homologous responses to selective pressures. This
391
collectiveness most occur despite the pressures of local adaptation (St Clair, Mandel, and Vance-
392
Borland, 2005) and drift. We present the idea that a varietal complex is an array of populations
393
where the processes that promote collective evolution are giving way to more localized
394
processes. The lack of distinctiveness to the varieties of A. lentiginosus are demonstrative of the
395
collective processes that have historically help this group together. Yet the great amount of
396
diversity and climatic correlations suggest the group is beginning to diverge due to local
397
processes. Further research is required to substantiate these claims but the foundations for these
Knaus, Cronn and Liston 19
398
claims have been set with this empirical investigation into the phenotypic divergence within this
399
group.
400
Knaus, Cronn and Liston 20
401
402
403
404
405
406
407
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520
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521
522
523
Knaus, Cronn and Liston 26
524
525
Table 1. Species of North American plants with 10 or more infrataxa (USDA, NRCS, 2007).
Family
Fabaceae
Polygonaceae
Asteraceae
Asteraceae
Malvaceae
Polygonaceae
Asteraceae
Asteraceae
Brassicaceae
Asteraceae
Caryophyllaceae
Fabaceae
Rosaceae
Asteraceae
Brassicaceae
Fabaceae
Onagraceae
Polygonaceae
Polygonaceae
526
527
528
529
Scientific Name
Astragalus lentiginosus
Eriogonum umbellatum
Ericameria nauseosa
Hymenopappus filifolius
Sidalcea malviflora
Eriogonum nudum
Ericameria parryi
Eriophyllum lanatum
Lepidium montanum
Achillea millefolium
Arenaria congesta
Trifolium longipes
Potentilla glandulosa
Machaeranthera canescens
Descurainia pinnata
Oxytropis campestris
Camissonia claviformis
Eriogonum heermannii
Eriogonum ovalifolium
Infra-rank
var.
var.
ssp. & var.
var.
ssp.
var.
var.
var.
var.
var.
var.
ssp.
ssp.
ssp. & var.
ssp.
var.
ssp.
var.
var.
count
35
30
22
13
13
13
12
12
12
11
11
11
11
10
10
10
10
10
10
Note: There are 33,383 species in the PLANTS database, 1,330 subspecies, and 2,523 varieties.
Knaus, Cronn and Liston 27
530
531
532
Table 2. The varieties of Astragalus lentiginosus (USDA, NRCS, 2007), sampled taxa are in
bold.
Variety
A. l. var. australis
A. l. var. borreganus
A. l. var. kennedyi
A. l. var. nigricalycis
A. l. var. palansb
A. l. var. variabilis
A. l. var. ambiguus
A. l. var. coachellae
A. l. var. maricopae
A. l. var. micans
A. l. var. stramineus
A. l. var. vitreus
A. l. var. yuccanus
A. l. var. araneosusc
A. l. var. chartaceus
A. l. var. diphysus
A. l. var. higginsii
A. l. var. idriensis
A. l. var. latus
A. l. var. oropedii
A. l. var. piscinensis
A. l. var. pohlii
A. l. var. sesquimetralis
A. l. var. wilsonii
A. l. var. floribundus
A. l. var. fremontii
A. l. var. ineptus
A. l. var. lentiginosus
A. l. var. salinus
A. l. var. albifolius
A. l. var. antonius
A. l. var. kernensis
A. l. var. scorpionis
A. l. var. semotus
A. l. var. sierrae
A.l. var. trumbellensis
36 varieties
533
534
535
536
537
538
539
Section
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Coulteriana
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Diphysa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Lentiginosa
Distribution
widespread
widespread
widespread
widespread
widespread
widespread
endemic
endemic
endemic
endemic
endemic
endemic
endemic
widespread
widespread
widespread
endemic
endemic
endemic
endemic
endemic
endemic
endemic
endemic
widespread
widespread
widespread
widespread
widespread
endemic
endemic
endemic
endemic
endemic
endemic
endemic
Barneby's
Samplea
31
31
31
56
40
114
4
34
5
5
9
16
16
39
55
66
NA
24
5
7
NA
NA
1
16
26
101
23
73
80
16
8
8
26
14
18
NA
998
Barneby's
Specimensa
5
4
3
2
9
9
1
2
0
0
1
2
3
8
8
10
NA
1
1
0
NA
NA
0
2
2
14
2
3
10
3
0
0
1
0
2
NA
108
Current
Sample
NA
19
19
NA
20
21
NA
20
NA
NA
NA
NA
NA
20
10
16
NA
NA
NA
NA
NA
NA
NA
NA
14
21
21
13
20
NA
NA
NA
10
NA
NA
NA
244
Notes:
This study includes 14 varieties.
a
Barneby (1964) reports the number of specimens he viewed in preparation of his monograph as
well as the number of specimens that were his own collections. Barneby is known for his
attention to detail, many of his own collections include drawings with measurements of key
characters. We believe these personal collections may represent the sample from which he
Knaus, Cronn and Liston 28
540
541
542
543
544
545
546
547
548
549
550
551
552
553
reports measurements in his monograph as opposed to the multitude which he may have only
viewed.
b
Rydberg (1929) placed many of what is currently known as A. lentiginosus in the two genera
Cystium and Tium. Here we have assigned A. l. var. palans to a section of Cystium in order to
treat A. lentiginosus as a group.
c
The variety araneosus is considered a synonym to var. diphysus in Barneby 1989 and the
PLANTS database, but was considered a valid taxon in Barneby 1964, the last comprehensive
treatment of A. lentiginosus.
d
Several varieties have been described since Rydberg’s 1929 treatment. Here we’ve taken
liberty to place these taxa as we feel Rydberg would have.
Knaus, Cronn and Liston 29
554
555
Table 3. Characters measured from specimens of Astragalus lentiginosus.
Character
Floral
peduncle length
Fl axis in fruit
keel length(mm)
calyx tooth length
calyx tube length
Fruit
pod length
pod height
pod valve thickness
beak length
Vegetative
Stem internode length
Leaf rachis length
Leaf petiole length
Leaflet number
Leaflet width
Leaflet length
556
557
558
Units
Transformation
0.5 mm
0.5 mm
0.5 mm
0.5 mm
0.5 mm
Na
Ln
Na
Na
Na
0.5 mm
0.5 mm
0.01 mm
0.5 mm
Na
Na
Ln
Na
0.5 mm
0.5 mm
0.5 mm
n
0.5 mm
0.5 mm
Na
Na
Na
Na
Na
Na
Knaus, Cronn and Liston 30
559
Table 4. Loadings on the first five principle components.
PC 1
Peduncle_length
Fl_axis_in_fruit
Keel_length.mm.
Pod_length
Pod_height
Pod_valve_thickness
Beak_length
Calyx_tooth_length
Calyx_tube_length
Stem_internode_length
Leaf_rachis_length
Leaf_petiole_length
Leaflet_number
Leaflet_width
Leaflet_length
560
0.3658
0.2937
0.2956
0.2543
0.0993
0.0866
0.0663
0.2741
0.2577
0.3047
0.3683
0.0242
0.0850
0.3381
0.3375
PC 2
PC 3
PC 4
PC 5
0.2069
0.3250
-0.3821
-0.2265
0.0835
-0.1807
-0.2751
-0.3029
-0.4654
0.2498
0.1681
0.0828
-0.2800
0.1692
0.1614
0.0409
0.0267
0.2145
-0.3597
-0.5256
0.4458
-0.5270
0.0415
0.0713
-0.0130
0.0536
-0.2333
-0.0470
0.0552
-0.0020
0.1855
0.2569
0.0518
-0.0146
-0.0238
-0.2919
-0.1199
-0.2239
0.0142
0.1416
0.1309
-0.3237
0.6515
-0.3395
-0.2540
0.0599
-0.0601
0.1036
-0.2220
0.0625
-0.0139
-0.2473
-0.0528
0.1306
-0.1239
0.1656
0.8459
0.2710
-0.0358
-0.1211
Knaus, Cronn and Liston 31
561
Fig. 1. Geographic distribution of sampled Astragalus lentiginosus. The distribution of A.
562
lentiginosus is primarily between the Rocky Mountains and the Sierra Nevada/Cascade Crest,
563
from British Columbia to Baja California Norte.
564
565
Fig. 2. Discriminant function analysis of morphometric data standardized by standard
566
deviations. Analysis was performed with (a) morphology as well as (b) morphology plus latitude
567
and longitude as explanatory factors of Barneby’s varieties (table 2). Grey scale corresponds to
568
Rydberg’s sections, white = Coulteriana, grey = Diphysa, Black = Lentiginosa.
569
570
Fig. 3. K-means clustering of data standardized by standard deviations. Lines represent the
571
optimality criteria Hartigan-Wong, Lloyd, Forgy, and MacQueen. Sum of squares for Rydberg’s
572
three sections and Barneby’s 14 varieties are provided for comparison.
573
574
Fig. 4. Simple linear regression of principle components one and two of morphometric data
575
against climatic parameters. Grey scale corresponds to Rydberg’s sections, white = Coulteriana,
576
grey = Diphysa, Black = Lentiginosa. PC1 is correlated to dormant season precipitation with R2
577
= 38% (F1, 196 = 123.7, p < 2.2e-16). PC2 is correlated to dormant season precipitation with R2 =
578
21% (F1, 174 = 47.23, p = 1.082e-10).
579
580
Fig. 5. Normal distributions of keel lengths plotted from the mean and variance of each variety
581
sampled (table 2). Using A. l. var. diphysus as a reference (μ = 11.5 mm, σ = 1.4 mm) the keel
582
lengths of A. lentiginosus span just over three standard deviations to A. l. var. lentiginosus (μ =
583
7.1 mm, σ = 0.6 mm).