Descendant Species Research Articles

Mechanical stress, fracture risk and beak evolution in Darwin's ground finches ( Geospiza )

Darwin's finches have radiated from a common ancestor into 14 descendent species, each specializing on distinct food resources and evolving divergent beak forms. Beak morphology in the ground finches (Geospiza) has been shown to evolve via natural selection in response to variation in food type, food availability and interspecific competition for food. From a mechanical perspective, however, beak size and shape are only indirectly related to birds' abilities to crack seeds, and beak form is hypothesized to evolve mainly under selection for fracture avoidance. Here, we test the fracture-avoidance hypothesis using finite-element modelling. We find that across species, mechanical loading is similar and approaches reported values of bone strength, thus suggesting pervasive selection on fracture avoidance. Additionally, deep and wide beaks are better suited for dissipating stress than are more elongate beaks when scaled to common sizes and loadings. Our results illustrate that deep and wide beaks in ground finches enable reduction of areas with high stress and peak stress magnitudes, allowing birds to crack hard seeds while limiting the risk of beak failure. These results may explain strong selection on beak depth and width in natural populations of Darwin's finches.

Parallelism in Evolution of Highly Repetitive DNAs in Sibling Species

Characterization of heterochromatin in the flour beetle Tribolium audax revealed two highly repetitive DNA families, named TAUD1 and TAUD2, which together constitute almost 60% of the whole genome. Both families originated from a common ancestral approximately 110-bp repeating unit. Tandem arrangement of these elements in TAUD1 is typical for satellite DNAs, whereas TAUD2 represents a dispersed family based on 1412-bp complex higher-order repeats composed of inversely oriented approximately 110 bp units. Comparison with repetitive DNAs in the sibling species Tribolium madens showed similarities in nucleotide sequence and length of basic repeating units and also revealed structural and organizational parallelism in tandem and dispersed families assembled from these elements. In both Tribolium species, one tandem and one dispersed family build equivalent distribution patterns in the pericentromeric heterochromatin of all chromosomes including supernumeraries. Differences in the nucleotide sequence and in the complexity of higher-order structures between families of the same type suggest a scenario according to which rearranged variants of the corresponding ancestral families were formed and distributed in genomes during or after the speciation event, following the same principles independently in each descendant species. We assume that random effects of sequence dynamics should be constrained by organizational and structural features of repeating units and possible requirements for spatial distribution of particular sequence elements. An interspersed pattern of repetitive families also points to the intensive recombination events in heterochromatin. Synergy between the meiotic bouquet stage and satellite DNA sequence dynamics could make a positive feedback loop that promotes the observed genome-wide distribution. At the same time, considering the abundance of these DNAs in heterochromatin spanning the (peri)centromeric chromosomal segments, we speculate that diverged repetitive sequences might represent the DNA basis of reproductive barrier between the two sibling species.

Greedy Selection of Species for Ancestral State Reconstruction on Phylogenies: Elimination Is Better than Insertion

Accurate reconstruction of ancestral character states on a phylogeny is crucial in many genomics studies. We study how to select species to achieve the best reconstruction of ancestral character states on a phylogeny. We first show that the marginal maximum likelihood has the monotonicity property that more taxa give better reconstruction, but the Fitch method does not have it even on an ultrametric phylogeny. We further validate a greedy approach for species selection using simulation. The validation tests indicate that backward greedy selection outperforms forward greedy selection. In addition, by applying our selection strategy, we obtain a set of the ten most informative species for the reconstruction of the genomic sequence of the so-called boreoeutherian ancestor of placental mammals. This study has broad relevance in comparative genomics and paleogenomics since limited research resources do not allow researchers to sequence the large number of descendant species required to reconstruct an ancestral sequence.

Evolutionary Mirages: Selection on Binding Site Composition Creates the Illusion of Conserved Grammars in Drosophila Enhancers

The clustering of transcription factor binding sites in developmental enhancers and the apparent preferential conservation of clustered sites have been widely interpreted as proof that spatially constrained physical interactions between transcription factors are required for regulatory function. However, we show here that selection on the composition of enhancers alone, and not their internal structure, leads to the accumulation of clustered sites with evolutionary dynamics that suggest they are preferentially conserved. We simulated the evolution of idealized enhancers from Drosophila melanogaster constrained to contain only a minimum number of binding sites for one or more factors. Under this constraint, mutations that destroy an existing binding site are tolerated only if a compensating site has emerged elsewhere in the enhancer. Overlapping sites, such as those frequently observed for the activator Bicoid and repressor Krüppel, had significantly longer evolutionary half-lives than isolated sites for the same factors. This leads to a substantially higher density of overlapping sites than expected by chance and the appearance that such sites are preferentially conserved. Because D. melanogaster (like many other species) has a bias for deletions over insertions, sites tended to become closer together over time, leading to an overall clustering of sites in the absence of any selection for clustered sites. Since this effect is strongest for the oldest sites, clustered sites also incorrectly appear to be preferentially conserved. Following speciation, sites tend to be closer together in all descendent species than in their common ancestors, violating the common assumption that shared features of species' genomes reflect their ancestral state. Finally, we show that selection on binding site composition alone recapitulates the observed number of overlapping and closely neighboring sites in real D. melanogaster enhancers. Thus, this study calls into question the common practice of inferring “cis-regulatory grammars” from the organization and evolutionary dynamics of developmental enhancers.

Implications of a fossil stickleback assemblage for Darwinian gradualism

Darwin postulated that a complete fossil record would contain numerous gradual transitions between ancestral and descendant species, but 150 years after publication of The Origin of Species, few such transitions have materialized. The fossil stickleback Gasterosteus doryssus and the deposit in which it occurs provide excellent conditions to detect such transitions. Abundant, well-preserved fossils occur in a stratigraphic setting with fine temporal resolution. The paleoecology of G. doryssus resembles the ecology of modern lakes that harbour the phenotypically similar three-spined stickleback Gasterosteus aculeatus. Gasterosteus aculeatus are primitively highly armoured, but G. doryssus comprised two contemporaneous biological species with relatively weak armour, including a near-shore, benthic feeder (benthic) and an offshore planktivore (limnetic). The benthic species expanded its range into the limnetic zone of the lake, where it apparently switched to planktivory and evolved reduced armour within c. 5000 years in response to directional selection. Although gradual evolution of mean phenotypes occurred, a single major gene caused much of evolutionary change of the pelvic skeleton. Thus, Darwin's expectation that transitions between species in the fossil record would be gradual was met at a fine time scale, but for pelvic structure, a well-studied trait, his expectation that gradual change would depend entirely on numerous, small, heritable differences among individuals was incorrect.

Das Triplett aus zwei Monophyla und einem Paraphylum als Baustein des phylogenetischen Systems

The triplet consisting of two monophyletic taxa and one paraphyletic taxon as constructive element of the phylogenetic system Evolution has produced very many novelties (apomorphies). Most of them are small and relatively inconstant, these are more or less indicative of the phylogenetic relationships between closely related species. They cannot be the constitutive character of a supraspecific taxon that exists since a long time and comprises many diversified species. Such a taxon of higher rank can only be characterized by an improbable, rare novelty that has developed only once and has been preserved in all descendent species. Two consecutive apomorphies of this persistent type (‘fixed apomorphies’) characterize three supraspecific taxa, the triplet “A”, “B” and “A minus B” (Fig. 1). The group “A minus B” is rejected in Hennig's theory because it is ‘paraphyletic’, but it is not an artefact created by the systematicist. It is an inevitable mathematical consequence of the differentiatison of the group “B” within the group “A”. Being the result of a subtraction, it is necessarily associated with the two monophyletic partners in the triplet, as it is delimited on one side by the synapomorphy of the group “A”, of which it is a part, and on the other side by the autapomorphy of the separate group “B”. Traditional classifications often include paraphyletic groupings that are inconsistent with phylogenetics, e. g. the Reptilia and the Apterygota. The fault in such cases is that these groups are extended beyond the limits of a triplet and cover more than a single interval between consecutive monophyletic taxa. Paraphyletic groups are admitted in the phylogenetic system only for bridging the gaps in our cladistic information. According to HENNIG'S theory, all supraspecific taxa should be arranged two by two as sister-groups originating from one ancestral species and comprising all descendents of that species. The fixed evolutionary novelties which characterize higher supraspecific taxa are, however, rare and scattered. It is highly improbable that they have developed in sister species, therefore the taxa marked by them cannot be sister-groups (except in very rare cases). In HENNIG'S earlier papers, e. g. in his system of Lepidoptera (1953: 46–49), the alleged ‘sister-groups' are, in reality, the groups “B” and “A minus B” of a triplet (see Fig. 2). In his revised concept (1957 and later), two autapomorphic groups which are most closely related in the recent fauna (“B” and “C” in Fig. 3) are called ‘sister-groups’. But these have originated independently from different ancestors in a plesiomorphic complex of extinct species and are more closely related to parts of this complex than to each other. True sister-groups (“Bx” and “Cx” in Fig. 4) would be formed if these related plesiomorphic species were included, but this extension of the ’backward‘ border of the taxon is not justified by synapomorphy (in the terms of logic, it is a ’metabasis‘), and it would make the classification of fossil species impossible, unless these show at least one synapomorphy with either “B” or “C”. In the system of the recent fauna the sister-groups are identical with the autapomorphic groups, because the plesiomorphic species are extinct. The natural system based on synapomorphies and autapomorphies is the triplet-system as outlined in Figure 6. It is not a new type of classification, but its theoretical foundation was missing, and precise instructions were needed for its use in phylogenetics. The information obtained by HENNIG'S method is entirely preserved in this system and can be retrieved from it, and both recent and extinct species can be classified together. The disadvantage of the triplet-system is that it contains twice as many taxa as HENNIG'S classification. This complexity will limit its use in the practice of taxonomy, but it may be simplified by transforming the system into a sequence of paraphyletic taxa terminating in a single monophylum.

Phenotypic Dimensions of Reproductive Isolation Between Northern and Melissa Blue Butterflies in the Rocky Mountains

Biological diversity results from speciation, which generally involves the splitting of an ancestral species into descendant species due to adaptation to different niches or the evolution of reproductive incompatibilities (Coyne and Orr 2004). The diverse flora and fauna of the world, including the native inhabitants of the Greater Yellowstone Area (GYA), exist as a result of the speciation process. The central role speciation plays in generating biological diversity imbues importance to our understanding of this process. The general importance of a thorough understanding of speciation is amplified because of the current high rates of extinction on the planet. This is because a long term solution to the present extinction crisis will require maintaining the processes that create species (speciation) not simply preventing extinction. However, many central questions regarding speciation remain to be answered. One fundamental question in speciation research is whether diverging species are isolated (i.e., prevented from interbreeding) due to differences in one, a few, or many characters and whether each of these character differences results from different alleles at a few or many genes. For example, speciation and reproductive isolation might involve divergence along multiple phenotypic axes, such as mate preference, habitat use or preference, and phenology (the timing of life-cycle events). Alternatively, isolation could result from differentiation of a single character. I propose to address this question by assessing patterns of variation for a suite of characters across a hybrid zone between two butterfly species. This is possible because patterns of character variation across hybrids zones allow for inferences about reproductive isolation (Barton and Hewitt 1985).

Casting an Eye on Complexity

In the previous issue, I offered some thoughts on how to think about evolution (Eldredge 2008). It turns out that how “we” collectively think about evolution, starting with the most basic, fundamental conceptualization about what evolution is, has differed dramatically depending on when a given evolutionist was active, what her subdiscipline is— and even to some degree on what country she was born in. For example, a systematist or paleontologist might prefer a one-sentence definition of “evolution” as “the idea that all species that have ever lived on earth are descended from a single common ancestor.” In contrast, a geneticist might prefer to define evolution as “any permanent change in genetic information.” In addition, while both definitions may suffice for some systematists or geneticists, others (such as myself) would insist on adding “and the causal processes underlying such patterns of descent and/or change in genetic information.” And while there may be still other definitions of evolution, these two seem to constitute a dichotomy that has pervaded biological evolutionary theory at least since Darwin. One of them is about the origin and fates of species—and, by extension, higher taxa such as genera, families etc. The other focuses on the origin and further modification of genetically based properties of organisms (morphology, physiology, behavior). And although such nondeterministic causes of genetic change as Sewall Wright’s “genetic drift” (see Eldredge 2008) are in operation, basically theories of genetic change (i.e., over and above mutational and related sorts of changes in individual organisms) are theories of adaptation through natural selection—and have been so throughout the history of evolutionary thought. What’s more, the distinction between these two fundamentally different ways of defining evolution—the “taxic” vs. the “transformationist” approach (as I initially called them in Eldredge 1979) are seldom acknowledged. The tendency (probably ever since Darwin published the Origin in 1859) is to see the “origin of species” as the simple and direct consequence of the ongoing transformation of the heritable properties of organisms via adaptation through natural selection. The thought goes: If natural selection modifies a species enough, over the course of time a new species will inevitably emerge. But, as I will explore in detail in the next issue (dedicated to Charles Robert Darwin on the occasion of his 200th birthday), Darwin himself initially saw evolution as a “taxic” phenomenon: ancestral species give rise to descendant species, much as mothers give birth to infant children. He was thinking in these terms even on the Beagle and continued to do so after he returned home in 1836. Later, he essentially dropped this line of thought—but only after he had come up with the idea of natural selection—and switched over to thinking of evolution as essentially the simple modification of adaptations through natural selection. Today, we have theories of “speciation”—how new species are “born” from ancestral species (see Thanukos 2008, for a useful review in these pages), and we also have theories of adaptation through natural selection. And it is clear that the two fundamentally different ways of thinking about evolution I have sketched out above are intimately related to one another: This is not an either/or dichotomy, but rather two equally valid ways of looking at evolution that resonate with one another in more of a dialectical than a dichotomous way. For though it is possible to have a descendant species arise with hardly much genetic change Evo Edu Outreach (2008) 1:355–357 DOI 10.1007/s12052-008-0070-7

SOME PROBLEMS WITH ASSESSING COPE'S RULE

Cope's Rule states that the size of species tends to increase along an evolutionary lineage. A basic statistical framework is elucidated for testing Cope's Rule and some surprising complications are pointed out. If Cope's Rule is formulated in terms of mean size, then it is not invariant to the way in which size is measured. If Cope's Rule is formulated in terms of median size, then it is not invariant to the degree of separation between ancestral and descendant species. Some practical problems in assessing Cope's Rule are also described. These results have implications for the empirical assessment of Cope's Rule.

MHC, TSP, and the Origin of Species: From Immunogenetics to Evolutionary Genetics

The acronym Mhc, major histocompatibility complex, is customarily not allied with topics in evolutionary biology. Here, however, we attempt to demonstrate that the Mhc has much to offer to this discipline and intimate that evolutionary biologists who ignore its contributions miss out on a chance of applying a new approach to vexing questions. One aspect of the Mhc in particular affords a fresh look at the population processes that transform one species into another: the trans-species polymorphism, the passage of allelic lineages from ancestral to descendant species. We provide examples of using the Mhc polymorphism in estimating the size of the founding population of new species, and of analyzing the long-term population demographies of phylogenetic lineages. We then extend the concept of trans-species polymorphism to other genes, even those not evolving under balancing selection, and argue that the phenomenon is widespread between closely related species. On the example of the cichlid fishes of Lake Victoria, we demonstrate how the concept changes the interpretation of this so-called "species flock." We contend that the conclusions reached regarding the cichlid fishes apply also to other examples of adaptive radiation, for example that of Darwin's finches, and so provide new insights into the nature of speciation in general.

INFERRING EVOLUTIONARY ORDER AND DURATIONS USING BOTH STRATIGRAPHY AND CLADISTICS IN A FOSSIL LINEAGE (BRYOZOA: PERONOPORA)

Abstract In the Ordovician bryozoan genus, Peronopora, stratigraphic occurrences and cladistic branching order are significantly correlated, indicating sequential development of both patterns in geological time. Five species have stratigraphic first appearances in the exact order predicted by cladistics, but eleven species require downward-range extensions to match cladistic order. Reduced major-axis regression-based corrections and ghost range extensions represent two alternative modifications of first appearance data, with the latter more strongly supported by stratigraphic congruence indices. Tests of the robustness of observed first appearances, based on the density of sampled horizons and magnitudes of stratigraphic gaps, support the probabilistic appearance of descendant species stratigraphically above their putative ancestors in eight of fifteen ancestor-descendant pairs. A 24 m sampling gap occurs below the base of the Brannon Member of the Lexington Limestone, a unit marking the first appearances...

The Joint Allele-Frequency Spectrum in Closely Related Species

We develop the theory for computing the joint frequency spectra of alleles in two closely related species. We allow for arbitrary population growth in both species after they had a common ancestor. We focus on the case in which a single chromosome is sequenced from one of the species. We use classical diffusion theory to show that, if the ancestral species was at equilibrium under mutation and drift and a chromosome from one of the descendant species carries the derived allele, the frequency spectrum in the other species is uniform, independently of the demographic history of both species. We also predict the expected densities of segregating and fixed sites when the chromosome from the other species carries the ancestral allele. We compare the predictions of our model with the site-frequency spectra of SNPs in the four HapMap populations of humans when the nucleotide present in the Neanderthal DNA sequence is ancestral or derived, using the chimp genome as the outgroup.

Geographical range size heritability: what do neutral models with different modes of speciation predict?

ABSTRACTAim Phylogenetic conservatism or heritability of the geographical range sizes of species (i.e. the tendency for closely related species to share similar range sizes) has been predicted to occur because of the strong phylogenetic conservatism of niche traits. However, the extent of such heritability in range size is disputed and the role of biology in shaping this attribute remains unclear. Here, we investigate the level of heritability of geographical range sizes that is generated from neutral models assuming no biological differences between species.Methods We used three different neutral models, which differ in their speciation mode, to simulate the life‐history of 250,000 individuals in a square lattice of 50 × 50 cells. These individuals can speciate, reproduce, migrate and die in the metacommunity according to stochastic events. We ran each model for 3000 steps and recorded the range size of each species at each step. The heritability of geographical range size was assessed using an asymmetry coefficient between range sizes of sister species and using the coefficient of correlation between the range sizes of ancestors and their descendants.Results Our results demonstrated the ability of neutral models to mimic some important observed patterns in the heritability of geographical range size. Consistently, sister species exhibited higher asymmetry in range sizes than expected by chance, and correlations between the range sizes of ancestor–descendant species pairs, although often weak, were almost invariably positive.Main conclusions Our findings suggest that, even without any biological trait differences, statistically significant heritability in the geographical range sizes of species can be found. This heritability is weaker than that observed in some empirical studies, but suggests that even here a substantial component of heritability may not necessarily be associated with niche conservatism. We also conclude that both present‐day and fossil data sets may provide similar information on the heritability of the geographical range sizes of species, while the omission of rare species will tend to overestimate this heritability.

Molecular phylogeny and biogeography of Picea (Pinaceae): Implications for phylogeographical studies using cytoplasmic haplotypes

The center of diversity is not necessarily the place of origin, as has been established by many plant molecular phylogenies. Picea is a complicated but very important genus in coniferous forests of the Northern Hemisphere, with a high species diversity in Asia. Its phylogeny and biogeography were investigated here using sequence analysis of the paternally inherited chloroplast trnC-trnD and trnT-trnF regions and the maternally inherited mitochondrial nad5 intron 1. We found that the North American P. breweriana and P. sitchensis were basal to the other spruces that were further divided into three clades in the cpDNA phylogeny, and that the New World species harbored four of five mitotypes detected, including two ancestral ones and three endemics. These results, combined with biogeographic analyses using DIVA and MacClade and fossil evidence, suggest that Picea originated in North America, and that its present distribution could stem from two times of dispersal from North America to Asia by the Beringian land bridge, and then from Asia to Europe. Most of the northeastern Asian species and the European P. abies could arise from a recent radiation given the very low interspecific genetic differentiation and pure mitotype of them. Considering that the ancestral mtDNA polymorphism can be preserved in many descendant species, even distantly related ones, we suggest that more species, at least the closely related ones, should be sampled in the phylogeographical study using cytoplasmic haplotypes if possible. In addition, we also discussed the evolution and phylogenetic utility of morphological characters in Picea.

Accumulation Phylogenies

Directed acyclic graphs provide a convenient representation of reticulate evolution in systematic biology. In this paper we formalize and analyse a simple model in which evolved characteristics are passed on to all descendant species. We show that the resulting observed sets of characteristics for the species at the leaves uniquely determine the digraph that described the evolution of the species, under certain restrictions. We also provide a characterisation for when this digraph is actually a tree.

USING HETEROCHRONY TO DETECT MODULARITY IN THE EVOLUTION OF STEM DIVERSITY IN THE PLANT FAMILY MORINGACEAE

Organisms are made up of semiautonomous parts or modules, but identifying the limits of modules is not straightforward. Covariation between morphological features across the adults of a clade can identify suites of characters as putative modules. We contrast such an approach for delimiting modules with one that includes inferences of heterochrony, evolutionary change in the timing of developmental events. That two features show differing types of heterochrony is a strong indication that they are ontogenetically dissociated and belong to differing modules even though these features may covary across adults. We focus on xylem vessels (wood water conduits) and phloem fibers (bark support cells) in the stems of the 13 species of the plant genus Moringa (Moringaceae), which vary from massive bottle trees to tiny tuberous shrubs. Across adults, vessel diameter and number of phloem fibers scale positively and significantly with stem size and with respect to one another. This covariation across adults suggests that these features may be members of the same ontogenetic module, a finding that might be expected given that these cells both derive from the same tissue ontogenetically and are tightly functionally integrated in the stem. In contrast, ontogenetic data in the context of a phylogenetic hypothesis suggest that vessel elements and phloem fibers have undergone different types of paedomorphosis, heterochronic alteration to ontogeny producing adults of descendant species that resemble the juveniles of their ancestors. Vessels and phloem fibers would be expected to show differing types of paedomorphosis only if they are not ontogenetically coupled, and therefore it is likely that they are part of different modules; this ontogenetic independence was invisible to inference based only on adult covariation. Finally, we show reasons to implicate paedomorphosis in the diversification in life form of Moringa across the Old World dry tropics.

Evolution of proteinase inhibitor defenses in North American allopolyploid species of Nicotiana

We studied the jasmonate (JA)-elicited trypsin-proteinase inhibitor (TPI) anti-herbivore defense system in North American Nicotiana to understand how complex polygenetic traits evolve after allopolyploidy speciation. N. quadrivalvis (Nq) and N. clevelandii (Nc) are allotetraploid descendant species of the ancestors of the diploid species N. attenuata (Na) and N. obtusifolia (No). From cDNA, intron and promoter sequence analyses, and Southern blotting, we deduced that only the maternally derived No TPI genes were retained in the tetraploid genomes (Nq, Nc), whereas the sequences of the paternal Na ancestor were deleted. The number of TPI repeats in different Nicotiana taxa was independent of phylogenetic associations. In Na, TPI activity and mRNA transcript accumulation as well as JA levels increased dramatically above wound-induced levels when the oral secretions (OS) from Manduca sexta larvae were introduced into wounds. This OS-mediated amplification of defense signaling and downstream response was also found in the tetraploid genomes but was absent from No; in No, OS treatment suppresses TPI mRNA accumulation and activity and does not increase JA accumulation. Hence, the tetraploids retained components of Na's signaling system, but lost Na's TPI genes and used No's TPI genes to retain a functional TPI defense system, underscoring the genomic flexibility that enables complex polygenic traits to be retained in allopolyploid species.

Hybrid origin of a swordtail species (Teleostei:Xiphophorus clemenciae) driven by sexual selection

The swordlike exaggerated caudal fin extensions of male swordtails are conspicuous traits that are selected for through female choice. Swords are one of only few examples where the hypothesis of a pre-existing bias is believed to apply for the evolution of a male trait. Previous laboratory experiments demonstrated that females prefer males with longer swords and even females from some swordless species show an affiliation for males of sworded species. Earlier phylogenetic studies based on maternally inherited mitochondrial DNA placed the sworded southern swordtail Xiphophorus clemenciae with swordless platies, contradicting its morphology-based evolutionary affinities. The analyses of new nuclear DNA markers now recover its traditional phylogenetic placement with other southern swordtails, suggesting that this species was formed by an ancient hybridization event. We propose that sexual selection through female choice was the likely process of hybrid speciation, by mating of platy females with males of an ancestral swordtail lineage. In artificial crosses of descendent species from the two potential ancestral lineages of X. clemenciae the hybrid and backcross males have swords of intermediate lengths. Additionally, mate choice experiments demonstrate that hybrid females prefer sworded males. These experimental lines of evidence make hybridization through xeno-specific sexual selection by female choice the likely mechanism of speciation.

USING HETEROCHRONY TO DETECT MODULARITY IN THE EVOLUTION OF STEM DIVERSITY IN THE PLANT FAMILY MORINGACEAE

Organisms are made up of semiautonomous parts or modules, but identifying the limits of modules is not straightforward. Covariation between morphological features across the adults of a clade can identify suites of characters as putative modules. We contrast such an approach for delimiting modules with one that includes inferences of heterochrony, evolutionary change in the timing of developmental events. That two features show differing types of heterochrony is a strong indication that they are ontogenetically dissociated and belong to differing modules even though these features may covary across adults. We focus on xylem vessels (wood water conduits) and phloem fibers (bark support cells) in the stems of the 13 species of the plant genus Moringa (Moringaceae), which vary from massive bottle trees to tiny tuberous shrubs. Across adults, vessel diameter and number of phloem fibers scale positively and significantly with stem size and with respect to one another. This covariation across adults suggests that these features may be members of the same ontogenetic module, a finding that might be expected given that these cells both derive from the same tissue ontogenetically and are tightly functionally integrated in the stem. In contrast, ontogenetic data in the context of a phylogenetic hypothesis suggest that vessel elements and phloem fibers have undergone different types of paedomorphosis, heterochronic alteration to ontogeny producing adults of descendant species that resemble the juveniles of their ancestors. Vessels and phloem fibers would be expected to show differing types of paedomorphosis only if they are not ontogenetically coupled, and therefore it is likely that they are part of different modules; this ontogenetic independence was invisible to inference based only on adult covariation. Finally, we show reasons to implicate paedomorphosis in the diversification in life form of Moringa across the Old World dry tropics.

Nodes in Phylogenetic Trees: The Relation Between Imbalance and Number of Descendent Species

The imbalance of a node in a phylogenetic tree can be defined in terms of the relative numbers of species (or higher taxa) on the branches that originate at the node. Empirically, imbalance also turns out to depend on the absolute total number of species on the branches: in a sample of large trees, nodes with more descendent species tend to be more unbalanced. Subsidiary analyses suggest that this pattern is not a result of errors in tree estimation. Instead, the increase in imbalance with species is consistent with a cumulative effect of differences in diversification rates between branches. [Equal-rates Markov model; imbalance; phylogeny shape; proportional-to-distinguishable-arrangements model.].