Alexander N. Schmidt-Lebuhn

Fallacies and false premises—a critical assessment of the arguments for the recognition of paraphyletic taxa in botany

One of the central controversies in contemporary taxonomy and systematics revolves around whether to accept or to reject paraphyletic taxa. The present review is the result of a survey of the ongoing discussion in botany over the past ca. 15u2003years, and attempts to systematically and critically assess all individual arguments presented for the formal recognition of paraphyletic groups in the classification of life. Where arguments are found to be without merit, rebuttals are presented in the hope of excluding them from further discussion, which can then concentrate on those that have merit. Where arguments are found to be sound, their implications and possible solutions are discussed. The controversy around paraphyletic taxa can be broken down into three questions: whether their rejection or acceptance would lead to a classification better reflecting patterns of biological diversity and evolutionary history; whether their rejection or acceptance would lead to a more practical, useful and predictive classification; and whether their rejection is compatible with ranked and binary Linnaean taxonomy. All available arguments for paraphyletic taxa relating to the first question are demonstrated to be based on various logical fallacies or false premises, especially misunderstandings of the principles of phylogenetic systematics. The issue of usefulness is harder to resolve, as different classifications serve different needs. It is presumably unavoidable but also preferable that phylogenetic and non‐phylogenetic ways of classifying species continue to coexist, serving different needs. Finally, an insistence on monophyletic taxa is found to be incompatible with binary taxonomy under a set of very specific circumstances and assumptions whose presence and accuracy are not universally accepted.

Quantifying Phytogeographical Regions of Australia Using Geospatial Turnover in Species Composition

The largest digitized dataset of land plant distributions in Australia assembled to date (750,741 georeferenced herbarium records; 6,043 species) was used to partition the Australian continent into phytogeographical regions. We used a set of six widely distributed vascular plant groups and three non-vascular plant groups which together occur in a variety of landscapes/habitats across Australia. Phytogeographical regions were identified using quantitative analyses of species turnover, the rate of change in species composition between sites, calculated as Simpsons beta. We propose six major phytogeographical regions for Australia: Northern, Northern Desert, Eremaean, Eastern Queensland, Euronotian and South-Western. Our new phytogeographical regions show a spatial agreement of 65% with respect to previously defined phytogeographical regions of Australia. We also confirm that these new regions are in general agreement with the biomes of Australia and other contemporary biogeographical classifications. To assess the meaningfulness of the proposed phytogeographical regions, we evaluated how they relate to broad scale environmental gradients. Physiographic factors such as geology do not have a strong correspondence with our proposed regions. Instead, we identified climate as the main environmental driver. The use of an unprecedentedly large dataset of multiple plant groups, coupled with an explicit quantitative analysis, makes this study novel and allows an improved historical bioregionalization scheme for Australian plants. Our analyses show that: (1) there is considerable overlap between our results and older biogeographic classifications; (2) phytogeographical regions based on species turnover can be a powerful tool to further partition the landscape into meaningful units; (3) further studies using phylogenetic turnover metrics are needed to test the taxonomic areas.

Non-geographic collecting biases in herbarium specimens of Australian daisies (Asteraceae)

Biological collections are increasingly becoming databased and available for novel types of study. A possible limitation of these data, which has the potential to confound analyses based on them, is their biased composition due to non-random and opportunistic collecting efforts. While geographic biases are comparatively well studied and understood, very little attention has been directed at other potential biases. We used Asteraceae specimen data from Australia’s Virtual Herbarium to test for over- and under-representation of plants with specific morphology, phenology and status by comparing observed numbers of specimens against a null distribution of simulated collections. Strong collecting biases could be demonstrated against introduced plants, plants with green or brown inflorescences, and very small plants. Specimens belonging to species with very restricted areas of distribution were also found to be strongly underrepresented. A moderate bias was observed against plants flowering in summer. While spiny plants have been collected only about half as often as should be expected, much of this bias was due to nearly all of them also being introduced (thistles). When introduced species were analyzed alone, a negative effect of spines remained but was much more moderate. The effect of woody or herbaceous habit, other inflorescence colours, tall growth and size of the capitula was comparatively negligible. Our results indicate that care should be taken when relying on specimen databases or the herbaria themselves for studies examining phenology, resource availability for pollinators, or the distribution and abundance of exotic species, and that researchers should be aware of collecting biases against small and unattractively coloured plants.

Phylogenetic relationships of the Australasian shrubby everlastings Ozothamnus and Cassinia (Asteraceae: Asteroideae: Gnaphalieae)

The first comprehensive phylogenetic study of the Australasian shrubby everlastings Ozothamnus, Cassinia, and their satellite genera is presented based on the nuclear ribosomal external and internal transcribed spacer and three chloroplast spacer regions (matK‐psbA, psbA‐trnH, ycf6‐pbsM). While the hypothesis of the monophyly of the sequence copies found in Cassinia cannot be rejected, sequences from Ozothamnus are found to be non‐monophyletic in three possible taxonomic circumscriptions of that genus. Cassinia, Calomeria, Odixia and Haeckeria are nested in a narrowly circumscribed Ozothamnus. Ozothamnus section Hebelaena, a sub‐shrubby group long recognized as potentially misplaced in the genus, is more heterogeneous than expected and is found to be potentially polyphyletic. Perhaps more surprisingly, a group of four species previously considered part of “core” Ozothamnus is found to be more closely related to other genera. It includes the subalpine “cascade everlastings” of south‐eastern Australia. Although many characters traditionally used for the delimitation of genera are homoplasious, connivent involucral bracts and presence of paleae are synapomorphies for Cassinia. Except for the robust shrubby habit, no morphological synapomorphy for core Ozothamnus/Cassinia is currently evident. Future studies are needed to test these results with additional data, to identify morphological and anatomical synapomorphies for individual clades and to resolve species‐level relationships with more extensive sampling to address the possibilities of incomplete lineage sorting or reticulate evolution.

Both morph- and species-dependent asymmetries affect reproductive barriers between heterostylous species

Abstract The interaction between floral traits and reproductive isolation is crucial to explaining the extraordinary diversity of angiosperms. Heterostyly, a complex floral polymorphism that optimizes outcrossing, evolved repeatedly and has been shown to accelerate diversification in primroses, yet its potential influence on isolating mechanisms remains unexplored. Furthermore, the relative contribution of pre‐ versus postmating barriers to reproductive isolation is still debated. No experimental study has yet evaluated the possible effects of heterostyly on pre‐ and postmating reproductive mechanisms. We quantify multiple reproductive barriers between the heterostylous Primula elatior (oxlip) and P. vulgaris (primrose), which readily hybridize when co‐occurring, and test whether traits of heterostyly contribute to reproductive barriers in unique ways. We find that premating isolation is key for both species, while postmating isolation is considerable only for P. vulgaris; ecogeographic isolation is crucial for both species, while phenological, seed developmental, and hybrid sterility barriers are also important in P. vulgaris, implicating sympatrically higher gene flow into P. elatior. We document for the first time that, in addition to the aforementioned species‐dependent asymmetries, morph‐dependent asymmetries affect reproductive barriers between heterostylous species. Indeed, the interspecific decrease of reciprocity between high sexual organs of complementary floral morphs limits interspecific pollen transfer from anthers of short‐styled flowers to stigmas of long‐styled flowers, while higher reciprocity between low sexual organs favors introgression over isolation from anthers of long‐styled flowers to stigmas of short‐styled flowers. Finally, intramorph incompatibility persists across species boundaries, but is weakened in long‐styled flowers of P. elatior, opening a possible backdoor to gene flow through intramorph pollen transfer between species. Therefore, patterns of gene flow across species boundaries are likely affected by floral morph composition of adjacent populations. To summarize, our study highlights the general importance of premating isolation and newly illustrates that both morph‐ and species‐dependent asymmetries shape boundaries between heterostylous species.

“Evolutionary” classifications do not have any information content—a reply to Stuessy and Hörandl

Sir, With my recent review in this journal (Schmidt-Lebuhn, 2012) I aimed to provide an overview of the arguments advanced by proponents of the acceptance of paraphyletic taxa in the botanical literature, and to examine if any of them stood up to critical evaluation. In their response, Stuessy and H€ orandl (2013) make the case that paraphyly is a form of monophyly, that long branches provide a justification for the formal recognition of paraphyletic residues at the same level as a clade nested within them, that “evolutionary” classifications accepting paraphyletic taxa are superior to phylogenetic systems because they contain more information, and that phylogenetic systematics will be unable to accommodate the increased understanding of evolutionary processes likely to result from contemporary progress in molecular and analytical methodology. Their attempt to generate a productive conversation between the two sides in this controversy by elucidating their approach and the reasoning behind it can only be welcomed. However, I find none of the four claims listed above to be convincing: The first and third are simply factually wrong, the second is based on a static, ahistorical and anthropocentric understanding of biological diversity, and the fourth on misconceptions about the principles of phylogenetic systematics. To justify the acceptance of paraphyletic taxa, Stuessy and H€ orandl argue that “paraphyly is [...] a type of monophyly” and “obviously” very different from polyphyly because paraphyletic groups also have a common ancestor. It is, however, unclear to me how they arrive at the implied conclusion that polyphyletic groups do not have a common ancestor. The currently preferred assumption appears to be that any two randomly chosen species on Earth have a common ancestor. Consequently, there is very little difference between paraphyla and polyphyla (Farris, 1974; Platnick, 1977). It is trivially possible to select a nonmonophyletic group of extant species and call it either paraphyletic or polyphyletic merely by changing the inferred ancestral state of the character used to diagnose it. In a group of four plant species, two of them yellow-flowered and two of them white-flowered, with a phylogeny of {yellow {white {white, yellow}}}, parsimony reconstruction of ancestral states under the assumption of accelerated transformation would make the yellows polyphyletic and the whites paraphyletic. The assumption of delayed transformation would reverse the situation, demonstrating that both groups would be equally unnatural regardless of their paraor polyphyly. In contrast, monophyletic groups are clearly different from non-monophyletic groups because they contain all descendants of a common ancestor instead of an arbitrarily chosen subset (Nelson, 1971). Stuessy and H€ orandl further argue that a long branch between a paraphyletic “ancestral complex” and a “derivative taxon” provides justification for treating the two as separate taxa at the same level. Unfortunately, the existence of long branches is an illusion brought about by extinction and an incomplete knowledge of the fossil record. Evolution proceeds through gradual changes over long time periods—there are simply no long branches in evolutionary history. In practice, any newly discovered intermediate species and, especially, any intermediate fossil breaks the long branches suggested as a criterion for the acceptance of paraphyletic taxa, throwing such a classificatory approach into confusion. In addition, the perceived long branches or “evolutionary divergence” cited as a criterion by evolutionary systematists are generally based on a small but human eye-catching set of morphological characters. It has long been clear that strong divergence in one sample of characters is not consistently predictive of strong divergence in another sample (Farris, 1971), and indeed today there is ample evidence from across the Cladistics

Do soil and climate properties drive biogeography of the Australian proteaceae

AimsThe Proteaceae are a diverse family of approximately 80 genera and 1700 species with a mostly southern-hemisphere distribution. While distributional patterns of various subsets of the Proteaceae have been studied, no quantitative continental-scale study of species-level spatial biodiversity patterns of the Australian Proteaceae has been conducted. The aim of this study is to identify and examine patterns of distribution, diversity and endemism for the Proteaceae (at family, genera and species levels) of continental Australia and to investigate the environmental drivers for the observed patterns.MethodsUsing 151,899 herbarium records for 1179 Australian Proteaceae species, we investigate taxon richness, endemism, and compositional turnover along with climatic and soil correlates.ResultsSpecies richness and endemism was highest in the Southwest phytogeographical region, as well as the Atherton and Southeastern subregions. Genus richness was highest in the Northeastern and Atherton subregions. Highest species turnover occured in the Southwestern region and the Southeastern subregion while lowest species turnover occured in the Northern, Northern Desert and Eremaean regions. Over the entire continent, soil geochemistry and climate explain 37% of the variation in species turnover; however, in areas of high species richness, they account for >75% of the variation in species turnover.ConclusionsThese results suggest that the biogeographic patterns of the Proteaceae are impacted by climate and soils, where Proteaceae specialization has filled novel environmental niches associated with low nutrient and low water availability soils, particularly in southwestern Australia.

Reciprocal monophyly of Craspedia and Pycnosorus (Asteraceae, Gnaphalieae) and the problems of using ribosomal DNA at the lowest taxonomic levels

Abstract. n The reciprocal monophyly of Craspedia and Pycnosorus (Asteraceae, Gnaphalieae) is tested, with a phylogenetic analysis of ribosomal and chloroplast DNA. Although one species of the latter genus was not sampled, the results of the present study indicated that it is most likely monophyletic as opposed to paraphyletic with respect to Craspedia. Within Craspedia, deeper sampling results in the appearance of several species (C. aurantia, C. coolaminica, C. glabrata and C. variabilis) in both major Australian rDNA clades, indicating that the available molecular phylogenies have to be considered gene trees instead of species phylogenies. Additional studies using more independent loci and species-tree approaches are needed to resolve species relationships in the genus.

A quantitative study of morphology in Australian Craspedia (Asteraceae, Gnaphalieae)

Abstract. The first comprehensive quantitative study of morphological characters in all Australian species of the billy button genus Craspedia (Asteraceae, Gnaphalieae) is presented. Homogeneity analysis and pair-wise reclassification tests are used to test species circumscriptions under the genotypic-cluster concept. Although most species are supported, C. aurantia and C. jamesii do not form separate morphological clusters, and C. jamesii is reduced to a variety of C. aurantia. Although our results indicated that C. variabilis may be synonymous with C. glauca, we reserve judgment because of the small number of specimens of the latter species included in the present study. Other species were found to be less problematic; however, additional and more detailed studies will be needed to clarify the circumscription of various species with woolly leaf indumentum, in particular C. canens, C. coolaminica and C. macrocephala. A synopsis of all Australian species of Craspedia is presented, together with a preliminary key.

Species trees from consensus single nucleotide polymorphism (SNP) data: Testing phylogenetic approaches with simulated and empirical data

Datasets of hundreds or thousands of SNPs (Single Nucleotide Polymorphisms) from multiple individuals per species are increasingly used to study population structure, species delimitation and shallow phylogenetics. The principal software tool to infer species or population trees from SNP data is currently the BEAST template SNAPP which uses a Bayesian coalescent analysis. However, it is computationally extremely demanding and tolerates only small amounts of missing data. We used simulated and empirical SNPs from plants (Australian Craspedia, Asteraceae, and Pelargonium, Geraniaceae) to compare species trees produced (1) by SNAPP, (2) using SVD quartets, and (3) using Bayesian and parsimony analysis with several different approaches to summarising data from multiple samples into one set of traits per species. Our aims were to explore the impact of tree topology and missing data on the results, and to test which data summarising and analyses approaches would best approximate the results obtained from SNAPP for empirical data. SVD quartets retrieved the correct topology from simulated data, as did SNAPP except in the case of a very unbalanced phylogeny. Both methods failed to retrieve the correct topology when large amounts of data were missing. Bayesian analysis of species level summary data scoring the two alleles of each SNP as independent characters and parsimony analysis of data scoring each SNP as one character produced trees with branch length distributions closest to the true trees on which SNPs were simulated. For empirical data, Bayesian inference and Dollo parsimony analysis of data scored allele-wise produced phylogenies most congruent with the results of SNAPP. In the case of study groups divergent enough for missing data to be phylogenetically informative (because of additional mutations preventing amplification of genomic fragments or bioinformatic establishment of homology), scoring of SNP data as a presence/absence matrix irrespective of allele content might be an additional option. As this depends on sampling across species being reasonably even and a random distribution of non-informative instances of missing data, however, further exploration of this approach is needed. Properly chosen data summary approaches to inferring species trees from SNP data may represent a potential alternative to currently available individual-level coalescent analyses especially for quick data exploration and when dealing with computationally demanding or patchy datasets.