Adaptations and history

The historical definition of adaptations has come into wide use as comparative biologists have applied methods of phylogenetic analysis to a variety of evolutionary problems. Here we point out a number of difficulties in applying historical methods to the study of adaptation, especially in cases where a trait has arisen but once. In particular, the potential complexity of the genetic correlations among phenotypic traits, performance variables and fitness makes inferring past patterns of selection from comparative data difficult. A given pattern of character distribution may support many alternative hypotheses of mechanism. While phylogenetic data are limited in their ability to reveal evolutionary mechanisms, they have always been an important source of adaptive hypotheses and will continue to be so.     

On a functional-morphological approach to phylogenetic reconstruction: A critique

A method of phylogenetic reconstruction as proposed by a number of scientists of the Senckenberg Research Institute is discussed. The method is based on functional-morphological studies, the evolutionary adaptation principle of Bock and Von Wahlert (1965) and so-called model reconstruction. It is argued in this paper that direction of the adaptation process cannot be determined because of lack of knowledge about particular selective forces and that theories of model reconstruction are not open to contradiction in the sense of Popperian falsification. Although it has been claimed that the method provides the only valid directional argument for morphoclines in cladistic studies, it remains unclear how to proceed when morphoclines show contradictory polarities. Moreover, it is doubtful whether polarities of morphoclines can be determined independently of phylogenetic hypotheses, and also whether the use of multistate morphoclines is methodologically valid. By relying on a particular evolutionary theory, i.e. the neo-Darwinian theory, and consequently assigning natural selection as the major agent of directional progress, the Senckenburg method of phylogenetic reconstruction restricts itself to microevolutionary change and, therefore, cannot be used when other hypotheses on the evolutionary process appear to explain the speciation process more plausibly, i.e. hypotheses on macroevolution. Furthermore, it is an unproved statement that evolution always proceeds according to the principle of economy.     

The Evolution of Integration of Biological Systems: An Evolutionary Perspective through Studies on Cells, Tissues, and Organs

Biologists are integrating studies of morphology, development,physiology,and other disciplines in order to understand howspecies and lineages diversify and cope with their environments.An evolutionary perspective in such studies, including thoseof cells, tissues, and organs, is potentially useful for thestructure and analysis of such problems. Evolutionary biologyis the study of the history of evolution and the elucidationof its mechanisms. Comparative biology is the comparison ofa trait or traits in selected taxa, and may be, but need notbe, evolutionary in approach. A phylogenetic hypothesis is necessaryfor reconstruction of pattern in morphology, ecology, behavior,and other areas. Acquaintance with evolutionary and phylogeneticperspectives can guide selection of taxa for study and opennew approaches to analysis of data. Such an approach is notalways appropriate to problems in biology, but it could be utilizedbeneficially more frequently than is currently practiced. Studiesof cells, tissues, and organs may contribute to the constructionof new phylogenetic hypotheses and to analysis of patterns andmechanisms of change when pursued from an evolutionary perspective     

Recent developments in the analysis of comparative data

Comparative methods can be used to test ideas about adaptation by identifying cases of either parallel or convergent evolutionary change across taxa. Phylogenetic relationships must be known or inferred if comparative methods are to separate the cross-taxonomic covariation among traits associated with evolutionary change from that attributable to common ancestry. Only the former can be used to test ideas linking convergent or parallel evolutionary change to some aspect of the environment. The comparative methods that are currently available differ in how they manage the effects brought about by phylogenetic relationships. One method is applicable only to discrete data, and uses cladistic techniques to identify evolutionary events that depart from phylogenetic trends. Techniques for continuous variables attempt to control for phylogenetic effects in a variety of ways. One method examines the taxonomic distribution of variance to identify the taxa within which character variation is small. The method assumes that taxa with small amounts of variation are those in which little evolutionary change has occurred, and thus variation is unlikely to be independent of ancestral trends. Analyses are then concentrated among taxa that show more variation, on the assumption that greater evolutionary change in the character has taken place. Several methods estimate directly the extent to which ancestry can predict the observed variation of a character, and subtract the ancestral effect to reveal variation of phylogeny. Yet another can remove phylogenetic effects if the true phylogeny is known. One class of comparative methods controls for phylogenetic effects by searching for comparative trends within rather than across taxa. With current knowledge of phylogenies, there is a trade-off in the choice of a comparative method: those that control phylogenetic effects with greater certainty are either less applicable to real data, or they make restrictive or untestable assumptions. Those that rely on statistical patterns to infer phylogenetic effects may not control phylogeny as efficiently but are more readily applied to existing data sets.     

Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea)

We demonstrate that by formulating guidelines for evolutionary morphology the transparency, reproducibility, and intersubject testability of evolutionary hypotheses based on morphological data can be enhanced. The five main steps in our concept of evolutionary morphology are (i) taxon sampling, (ii) structural analysis, (iii) character conceptualization, (iv) phylogenetic analysis, and (v) evolutionary interpretation. We illustrate this concept on the example of the morphology of the circulatory organs in peracarid Malacostraca. The analysis is based on recently published accounts in which detailed structural analyses were carried out, and on the older literature. Detailed conceptualizations of 22 characters of the circulatory system are given for 28 terminals. In a further step these characters are included in a recently revised matrix, resulting in 110 characters. The resulting parsimony analysis yielded a single most parsimonious tree with a length of 309 steps. The most significant results are that Peracarida is monophyletic, Amphipoda is the sister taxon to the Mancoida sensu stricto, the relict cave‐dwelling taxa Thermosbaenacea, Spelaeogriphacea, and Mictocarididae form a monophylum and Tanaidacea is the sister group to a monophylum comprising Cumacea and Isopoda. The evolutionary analysis shows that the ground pattern features of the circulatory organs in Peracarida are a tubular heart extending through the whole thorax, a posterior aorta with lateral arteries, and a ventral vessel system. Important features within the Peracarida are the backward shift of the anterior border of the heart, the reduction of the ventral vessel system, and two patterns of cardiac arteries, one common to the amphipod and tanaidacean terminals, and one to the cumacean and isopod terminals. © The Willi Hennig Society 2009.     

On adaptation, the assessment of adaptations, and the value of adaptive arguments in phylogenetic reconstruction

Evolutionary adaptation concerns a relative concept and the study of adaptations is directed to structures of individuals. The concept is devoid of any meaning when it is applied to species or populations. Adaptation is not synonymous with fitness or survival but does contribute to both of them. The term adaptation has a dual meaning since it refers both to the process of adaptation and to the state of being adapted. In the process of adaptation the mechanism of natural selection takes a prominent position. But the operation and effectiveness of natural selection are constrained by various limiting factors. Besides that, features may also be the result of nonadaptive evolution and only attain their present adaptive function at a later point in time. Another possibility is that features have at present a function different from the one for which they were initially designed. With respect to the state of being, the study of adaptation attempts to examine whether a particular feature indeed forms an adequate response to selection forces from the environment. Five methods or approaches generally are used to assess the adaptive significance of features, viz. the comparative, correlation, optimization, cladistic, and synthetic approach. Only the last-mentioned approach forms an adequate method since it attempts to establish, by direct analysis, which well-defined selection force exerts its influence on a certain character. The practicing taxonomist is faced with the problem that the data necessary to apply the synthetic method, generally require detailed field studies. Not all evolutionary changes are under the influence of natural selection. The presence of some features may be based on entirely different mechanisms, such as genetic drift, mutational pressure, pleiotropic gene action, allometric growth, or ecophenotypic responses. Various problems inherent to the optimization approach, and several others of practical and theoretical nature, make the morphocline method of the functional and evolutionary morphologists unsuitable as a method for phylogenetic reconstruction.     

Testing adaptation with phylogeny: how to account for phylogenetic pattern and selective value together

If most agree with the dual pattern/process definition of adaptation, an apomorphy promoted by natural selection, few indeed identify an adaptation using the same methodological procedure. Most differences between procedures rest with the way the role of natural selection is analysed in a phylogenetic perspective. We argue that the selective value of a character cannot be phylogenetically reconstructed, but must be considered independently from the phylogenetic analysis in the framework of population biology. The phylogenetic pattern for the character of interest can only be used to refute or corroborate circumstantially the macro-evolutionary predictions issuing from population studies.     

Key Innovations: Further Remarks on the Importance of Morphology in Elucidating Systematic Relationships and Adaptive Radiations

The present paper is an argument in support of the continued importance of morphological systematics and a plea for improving molecular phylogenetic analyses by addressing explicit character transformations. We use here the inference of key innovations and adaptive radiations to demonstrate why morphological systematics is still relevant and necessary. After establishing that theories of phylogenetic relationship offer robust explanatory bases for discussing evolutionary diversification, the following topics are addressed: (1) the inference of key innovations grounded in phylogenetic analyses; (2) the epistemic distinction between character ‘mapping’ and relevant evidence in systematic and evolutionary studies; and (3) key innovations in molecular phylogenetics. We emphasize that the discovery of key innovations, in fossil or extant taxa, further strengthens the importance of morphology in systematic and evolutionary inferences, as they reveal scenarios of character transformation that have led to asymmetrical sister-group diversification. Our main conclusion is that understanding characters in and of themselves, when properly contextualized systematically, is what evolutionary biologists should be concerned with, whereas the analysis of tree topology alone, in which statistical nodal support measures are the sole indicators of phylogenetic affinity, does not lead to a fuller understanding of key innovations.     

The Role of Functional Analysis in Phylogenetic Inference: Examples from the History of the Xiphosura

SYNOPSIS. Conventional cladistic analyses of phylogeny can beinterpreted as operating at the level of phylogenetic trees.They assume that all "evolutionary steps" (transitions fromone character state to the next, along a morphocline) are independentand equal, and, on that basis, select the cladogram which isconsistent with the most parsimonious trees. Evaluation of theassumptions of independence and equality requires considerationof hypotheses at the levelof scenarios. In some cases, argumentsbased on functional analysis can suggest revised interpretationsof either homology or polarity. If properly formulated, thesearguments can alter the evaluation of parsimony for trees tothe extent that even the choice of cladogram is affected. Thestructure of scenario level arguments is identical to that ofarguments operating at tree level. Examples of phylogeneticinference in the context of xiphosurans (horseshoe crabs), usingboth comparative morphological and functional analysis, illustratethis approach. In different cases, orthodox interpretationsof relationship are either challenged or corroborated. Althoughthe introduction of functional analysis into the process ofphylogenetic inference may appear to compromise the usefulnessof the reconstructed phylogeny for testing hypotheses concerningthe role of natural selection in evolution, it actually increasesthe strength of such tests.     

Cladistic Analysis of Human Evolution: Some Points on Character Selection

Cladistic analysis strongly depends on accurate character choice. Usually, characters include morphology or molecules, but other sources of evidence are also employed. These include stratigraphic ages of taxa and behavioural data. The inclusion of time is a controversial issue, which has no Darwinian basis. However, the cladistic treatment of stratigraphic age has the potential to resolve problematic phylogenies. Here, it is proposed that the use of stratigraphic data in phylogenetic inference should be seen as a temporary shortcut, to resolve complex phylogenies in the wait for new character and taxonomic samplings, because phylogenetic hypotheses should be based on biological evidence only. Archaeologists working on toolmaking can provide behavioural data in human prehistory. In fact, while a tool itself is not biological evidence, the movements of hands and arms needed to prepare it are biological evidence and can be compared and scored for cladistic analysis. Such an approach has been formalized in studies on functional morphology of some vertebrates. The taxonomic data set to be used in cladistic analysis should include as many taxa as possible, and also very incomplete specimens should be used. In many cases, incomplete specimens had the potential to resolve complex phylogenies by adding new character combinations that cannot be scored in molecule-based phylogenetic studies.     

The phylogenetic position of the Clitellata and the Echiura - on the problematic assessment of absent characters*

Absent characters (negative characters) are difficult to assess and their correct interpretation as symplesiomorphies, synapomorphies or convergencies (homoplasies) is one of the greatest challenges in phylogenetic systematics. Different phylogenetic assessments often result in contradictory phylogenetic hypotheses, in which the direction of evolutionary changes is diametrically opposed. Especially in deciding between primary (plesiomorphic) and secondary (apomorphic) absence, false conclusions may be reached if only the outgroup comparison and the principle of parsimony are employed without attempting any biological evaluation or interpretation of characters. For example, in the higher‐level systematization of the Annelida and related taxa different assessments of absent characters have led to conflicting hypotheses about the phylogenetic relationships and the ground pattern of the annelid stem species. Varying phylogenetic interpretations regarding the absence of the chemosensory nuchal organs in the clitellates and their presence in polychaetes initiated a controversy that produced two alternative phylogenetic hypotheses: (1) the Clitellata are highly derived Annelida related to a subtaxon within the, in this case, paraphyletic ‘Polychaeta’ or (2) the Clitellata are comparatively primitive Annelida representing the sister group of a monophyletic taxon Polychaeta. In the former, the absence of nuchal organs in the Clitellata is regarded as a secondary character, in the latter as primary. As most Clitellata are either limnetic or terrestrial, we must ask which characters are plesiomorphies, taken from their marine stem species without changes. In addition to a thorough investigation and evaluation of clitellate characters, a promising approach to these questions is to look for such characters in limnetic and terrestrial annelids clearly not belonging to the Clitellata. A similar problem applies to the evaluation of the position of the Echiura, which lack both segmentation and nuchal organs. Evidence is presented that in both taxa these absent characters represent derived, apomorphic character states. The consequences for their phylogenetic position and the questionable monophyly of the Polychaeta are discussed. The conclusion drawn from morphological character assessments is in accordance with recently published hypotheses based on molecular data.     

Comparative methods for examining adaptation depend on evolutionary models

Comparisons among taxa provide a powerful means for helping to understand why primate species differ from each other in morphology, behaviour and life history. Comparative tests can also mislead when not applied correctly, and correct application means taking into account the phylogenetic relationships among the species being compared. Adaptation is defined as a comparative concept. The reasons for phenotypic similarity among closely related taxa are summarized. Different models of evolutionary change dictate different methods for reconstructing ancestral character states and for performing comparative analyses on categorical and continuously varying character. All comparative methods rely either implicitly of explicitly on some model of how evolution proceeds. The choice of a particular method of analysis is, therefore, an implicit choice of a model of evolution.     

Adaptation and functional integration in primate phylogenetics

In two areas of phylogenetics, contrary predictions have been developed and maintained for character analysis and weighting. With regard to adaptation, many have argued that adaptive characters are poorly suited to phylogenetic analysis because of a propensity for homoplasy, while others have argued that complex adaptive characters should be given high weight because homoplasy in complex characters is unlikely. Similarly, with regard to correlated sets of characters, one point of view is that such sets should be collapsed into a single character-a single piece of phylogenetic evidence. Another point of view is that a suite of correlated characters should be emphasized in phylogenetics, again because recurrence of detailed similarity in the same suite of features is unlikely. In this paper, I discuss the theoretical background of adaptation and functional integration with respect to phylogenetic systematics of primates. Several character examples are reviewed with regard to their functional morphology and phylogenetic signal: postorbital structures, tympanic morphology, fusion of the mandibular symphysis, the tooth comb, strepsirrhine talar morphology, and the prehensile tail. It is clear when considering characters such as these that some characters are synapomorphic of major clades and at the same time functionally important. This appears particularly to be the case when characters are integrated into a complex and maintained as stable configurations. Rather than being simply a problem in character analysis, processes of integration may help to explain the utility of phylogenetically informative characters. On the other hand, the character examples also highlight the difficulty in forming a priori predictions about a character's phylogenetic signal. Explanations of patterns of character evolution are often clade-specific, which does not allow for a simple framework of character selection and/or weighting.     

Finding Optimal Ingroup Topologies and Convexities When the Choice of Outgroups Is Not Obvious

Considerable confusion remains among theoreticians and practicioners of phylogenetic science on the use of outgroup taxa. Here, we show that, despite claims to the contrary, details of the optimal ingroup topology can be changed by switching outgroup taxa. This has serious implications for phylogenetic accuracy. We delineate between the process of outgroup selection and the various possible processes involved in using an outgroup taxon after one has been selected. Criteria are needed for the determination that particular outgroup taxa do not reduce the accuracy of evolutionary tree topologies and inferred character state transformations. We compare previous results from a sensitivity bootstrap analysis of the mitochondrial cytochromebphylogenetic relationships among whales to the results of a Bremer support sensitivity analysis and of a recently developed application of RASA theory to the question of putative outgroup taxon plesiomorphy content.     

Mosaics of convergences and noise in morphological phylogenies: what's in a viverrid-like carnivoran?

Adaptive convergence in morphological characters has not been thoroughly investigated, and the processes by which phylogenetic relationships may be misled by morphological convergence remains unclear. We undertook a case study on the morphological evolution of viverrid-like feliformians (Nandinia, Cryptoprocta, Fossa, Eupleres, Prionodon) and built the largest morphological matrix concerning the suborder Feliformia to date. A total of 349 characters grouped into four anatomical partitions were used for all species of Viverridae and viverrid-like taxa plus representatives of the Felidae, Hyaenidae, Herpestidae, and one Malagasy mongoose. Recent molecular phylogenetic analyses suggest that viverrid-like morphotypes appeared independently at least three times during feliformian evolution. We thus used a synthetic molecular tree to assess morphological evolutionary patterns characterizing the viverrid-like taxa. We examined phylogenetic signal, convergence and noise in morphological characters using (a) tree-length distribution (g1), (b) partitioned Bremer support, (c) RI values and their distribution, (d) respective contributions of diagnostic synapomorphies at the nodes for each partition, (e) patterns of shared convergences among viverrid-like taxa and other feliformian lineages, (f) tree-length differences among alternative hypotheses, and (g) the successive removal of convergent character states from the original matrix. In addition, the lability of complex morphological structures was assessed by mapping them onto the synthetic molecular tree. The unconstrained morphological analysis yielded phylogenetic groupings that closely reflected traditional classification. The use of a synthetic molecular tree (constraint) combined with our thorough morphological investigations revealed the mosaics of convergences likely to have contributed to part of the historical uncertainty over viverrid classification. It also showed that complex morphological structures could be subjected to reversible evolutionary trends. The morphological matrix proved useful in characterizing several feliformian clades with diagnostic synapomorphies. These results support the removal from the traditionally held Viverridae of several viverrid-like taxa into three distinct families: Nandiniidae (Nandinia), Prionodontidae (Prionodon), and the newly defined Eupleridae (including Cryptoprocta, Fossa, Eupleres plus all "mongoose-like" Malagasy taxa). No clearly "phylogenetically misleading" data subsets could be identified, and the great majority of morphological convergences appeared to be nonadaptive. The multiple approaches used in this study revealed that the most disruptive element with regards to morphological phylogenetic reconstruction was noise, which blured the expression of phylogenetic signal. This study demonstrates the crucial need to consider independent (molecular) phylogenies in order to produce reliable evolutionary hypotheses and should promote a new approach to the definition of morphological characters in mammals. [Constrained analysis; convergence; evolutionary scenario; Feliformia; morphology; noise; phylogenetic signal; phylogeny; Viverridae.].     

Genomic biodiversity, phylogenetics and coevolution in proteins

Comprehensive sampling of genomic biodiversity is fast becoming a reality for some genomic regions and complete organelle genomes. Genomic biodiversity is defined as large genomic sequences from many species, and here some recent work is reviewed that demonstrates the potential benefits of genomic biodiversity for molecular evolutionary analysis and phylogenetic reconstruction. This work shows that using likelihood-based approaches, taxon addition can dramatically improve phylogenetic reconstruction. Features or dynamics of the evolutionary process are much more easily inferred with large numbers of taxa, and large numbers are essential for discriminating differences in evolutionary patterns between sites. Accurate prediction of site-specific patterns can improve phylogenetic reconstruction by an amount equivalent to quadrupling sequence length. Genomic biodiversity is particularly central to research relating patterns of evolution, adaptation and coevolution to structural and functional features of proteins. Research on detecting coevolution between amino acid residues in proteins demonstrates a clear need for much greater numbers of closely related taxa to better discriminate site-specific patterns of interaction, and to allow more detailed analysis of coevolutionary interactions between subunits in protein complexes. It is argued that parsing out coevolutionary and other context-dependent substitution probabilities is essential for discriminating between coevolution and adaptation, and for more realistically modelling the evolution of proteins. Also reviewed is research that argues for increasing the efficiency of acquiring genomic biodiversity, and suggests that this might be done by simultaneously shotgun cloning and sequencing genomic mixtures from many species. Increased efficiency is a prerequisite if genomic biodiversity levels are to rapidly increase by orders of magnitude, and thus lead to dramatically improved understanding of interactions between protein structure, function and sequence evolution.     

Circularity and Independence in Phylogenetic Tests of Ecological Hypotheses

It has been asserted that in order to avoid circularity in phylogenetic tests of ecological hypotheses, one must exclude from the cladistic analysis any characters that might be correlated with that hypothesis. The argument assumes that selective correlation leads to lack of independence among characters and may thus bias the analysis. This argument conflates the idea of independence between the ecological hypothesis and the phylogeny with independence among characters used to construct the tree. We argue that adaptation or selection does not necessarily result in the non-independence of characters, and that characters for a cladistic analysis should be evaluated as homology statements rather than functional ones. As with any partitioning of data, character exclusion may lead to weaker phylogenetic hypotheses, and the practice of mapping characters onto a tree, rather than including them in the analysis, should be avoided. Examples from pollination biology are used to illustrate some of the theoretical and practical problems inherent in character exclusion.     

Mapping cladograms into morphospaces

In cladistic analyses, taxa are grouped hierarchically into clades according to shared apomorphic character states to construct cladograms; cladograms are interpretable as phylogenetic hypotheses. In morphological space analyses, organism forms are represented as points in morphospaces; point proximities in morphospaces represent similarities that might be attributable to phenetic convergence and, consequently, may correspond inaccurately with hypothesized evolutionary relationships. A method for synthesizing phylogenetic results that are interpreted from cladistic analyses with phenetic results that are obtained from morphological space analyses is presented here; in particular, points that represent forms typifying taxa in morphospace are assigned as terminal nodes for appropriate cladograms that are mapped into morphospaces by positioning nonterminal nodes and orienting internodes according to a geometric algorithm. Nonterminal nodes may be interpreted as ancestors in phylogenetic hypotheses and occupy positions that represent particular organism forms in morphospaces. By mapping cladograms into morphospaces, therefore, evolutionary morphologists can reconstruct ancestral morphologies and test historical transformation hypotheses.     

Complete cpDNA genome sequence of Smilax china and phylogenetic placement of Liliales--influences of gene partitions and taxon sampling

The complete nucleotide sequence of the chloroplast genome (cpDNA) of Smilax china L. (Smilacaceae) is reported. It is the first complete cp genome sequence in Liliales. Genomic analyses were conducted to examine the rate and pattern of cpDNA genome evolution in Smilax relative to other major lineages of monocots. The cpDNA genomic sequences were combined with those available for Lilium to evaluate the phylogenetic position of Liliales and to investigate the influence of taxon sampling, gene sampling, gene function, natural selection, and substitution rate on phylogenetic inference in monocots. Phylogenetic analyses using sequence data of gene groups partitioned according to gene function, selection force, and total substitution rate demonstrated evident impacts of these factors on phylogenetic inference of monocots and the placement of Liliales, suggesting potential evolutionary convergence or adaptation of some cpDNA genes in monocots. Our study also demonstrated that reduced taxon sampling reduced the bootstrap support for the placement of Liliales in the cpDNA phylogenomic analysis. Analyses of sequences of 77 protein genes with some missing data and sequences of 81 genes (all protein genes plus the rRNA genes) support a sister relationship of Liliales to the commelinids-Asparagales clade, consistent with the APG III system. Analyses of 63 cpDNA protein genes for 32 taxa with few missing data, however, support a sister relationship of Liliales (represented by Smilax and Lilium) to Dioscoreales-Pandanales. Topology tests indicated that these two alignments do not significantly differ given any of these three cpDNA genomic sequence data sets. Furthermore, we found no saturation effect of the data, suggesting that the cpDNA genomic sequence data used in the study are appropriate for monocot phylogenetic study and long-branch attraction is unlikely to be the cause to explain the result of two well-supported, conflict placements of Liliales. Further analyses using sufficient nuclear data remain necessary to evaluate these two phylogenetic hypotheses regarding the position of Liliales and to address the causes of signal conflict among genes and partitions.