Ontogeny discombobulates phylogeny: paedomorphosis and higher-level salamander relationships

Evolutionary developmental biology ("evo-devo") has revolutionized evolutionary biology but has had relatively little impact on systematics. We show that similar large-scale developmental changes in distantly related lineages can dramatically mislead phylogenetic analyses based on morphological data. Salamanders are important model systems in many fields of biology and are of special interest in that many species are paedomorphic and thus never complete metamorphosis. A recent study of higher-level salamander phylogeny placed most paedomorphic families in a single clade based on morphological data. Here, we use new molecular and morphological data to show that this result most likely was caused by the misleading effects of paedomorphosis. We also provide a well-supported estimate of higher-level salamander relationships based on combined molecular and morphological data. Many authors have suggested that paedomorphosis may be problematic in studies of salamander phylogeny, but this hypothesis has never been tested with a rigorous phylogenetic analysis. We find that the misleading effects of paedomorphosis on phylogenetic analysis go beyond the sharing of homoplastic larval traits by paedomorphic adults, and the problem therefore is not solved by simply excluding suspected paedomorphic characters. Instead, two additional factors are critically important in causing paedomorphic species to be phylogenetically "misplaced": (1) the absence of clade-specific synapomorphies that develop during metamorphosis in nonpaedomorphic taxa and allow their "correct" placement and (2) parallel adaptive changes associated with the aquatic habitat of the larval stage. Our results suggest that the effects of paedomorphosis on phylogenetic analyses may be complex, difficult to detect, and can lead to results that are both wrong and statistically well supported by parsimony and Bayesian analyses.     

Molecular phylogeny of the three paedomorphic Mediterranean gobies (Perciformes: Gobiidae)

Pelagic gobies are considered of particular zoological interest because the acquisition of a pelagic lifestyle is achieved through the persistence of larval anatomical features. The Mediterranean Sea is inhabited by three goby species (Aphia minuta, Crystallogobius linearis and Pseudaphya ferreri) characterized by paedomorphic traits. Owing to the shared larval morphological features, these species have generally been considered as a monophyletic group. This study aimed at establishing the phylogenetic relationships of these paedomorphic species within the family Gobiidae to ascertain whether the pelagic lifestyle achieved through paedomorphosis is due to an event that took place in a common ancestor or not. For this purpose, we amplified by polymerase chain reaction and sequenced the mitochondrial 12S rDNA (complete sequence) and 16S rDNA (partial sequence) of 15 Mediterranean gobies. The phylogenetic analysis strongly supported the polyphyletic origin of the three paedomorphic gobies, indicating that the heterochronic change leading to the retention of larval features seems to have occurred independently in the ancestors of these species. Thus, the sharing of morphological traits can be considered homoplasious and the classification of these species in the same taxonomic group is rejected on the basis of molecular data.     

The role of character loss in phylogenetic reconstruction as exemplified for the Annelida

Annelid relationships are controversial, and molecular and morphological analyses provide incongruent estimates. Character loss is identified as a major confounding factor for phylogenetic analyses based on morphological data. A direct approach and an indirect approach for the identification of character loss are discussed. Character loss can frequently be found within annelids and examples of the loss of typical annelid characters, like chaetae, nuchal organs, coelomic cavities and other features, are given. A loss of segmentation is suggested for Sipuncula and Echiura; both are supported as annelid ingroups in molecular phylogenetic analyses. Moreover, character loss can be caused by some modes of heterochronic evolution (paedomorphosis) and, as shown for orbiniid and arenicolid polychaetes, paedomorphic taxa might be misplaced in phylogenies derived from morphology. Different approaches for dealing with character loss in cladistic analyses are discussed. Application of asymmetrical character state transformation costs or usage of a dynamic homology framework represents promising approaches. Identifying character loss prior to a phylogenetic analysis will help to refine morphological data matrices and improve phylogenetic analyses of annelid relationships.     

Population structure and genetic diversity of metamorphic and paedomorphic populations of the tiger salamander,Ambystoma tigrinum

Genetic relationships, population subdivision and genetic diversity were estimated from mtDNA and allozyme data for two subspecies of tiger salamander, one of which is obligately metamorphic and the other polymorphic for paedomorphosis (larval reproduction). Far greater genetic differentiation exists between subspecies than within subspecies, suggesting that the subspecies have evolved in allopatry. Values of F_st calculated from both mtDNA and allozymes were greater than 0.400 for each subspecies. Significant population subdivision was detected even on a microgeographic scale. This extensive population subdivision indicates that populations can respond to extremely localized selection pressures. In the case of paedomorphosis, populations in permanent water should evolve paedomorphosis as long as the appropriate genes exist. For both mtDNA and allozymes, comparisons of population structure within the polymorphic subspecies and between polymorphic and metamorphic subspecies reveal no discernible effects of paedomorphosis. However, a comparison of paedomorphic and metamorphic populations of the polymorphic subspecies showed significantly higher mtDNA diversity in paedomorphic populations. The discrepancy between the allozyme and mtDNA results may be due to the lower effective population size of mtDNA compared to autosomal genes.     

Failure of the ILD to determine data combinability for slow loris phylogeny

Tests for incongruence as an indicator of among-data partition conflict have played an important role in conditional data combination. When such tests reveal significant incongruence, this has been interpreted as a rationale for not combining data into a single phylogenetic analysis. In this study of lorisiform phylogeny, we use the incongruence length difference (ILD) test to assess conflict among three independent data sets. A large morphological data set and two unlinked molecular data sets--the mitochondrial cytochrome b gene and the nuclear interphotoreceptor retinoid binding protein (exon 1)--are analyzed with various optimality criteria and weighting mechanisms to determine the phylogenetic relationships among slow lorises (Primates, Loridae). When analyzed separately, the morphological data show impressive statistical support for a monophyletic Loridae. Both molecular data sets resolve the Loridae as paraphyletic, though with different branching orders depending on the optimality criterion or character weighting used. When the three data partitions are analyzed in various combinations, an inverse relationship between congruence and phylogenetic accuracy is observed. Nearly all combined analyses that recover monophyly indicate strong data partition incongruence (P = 0.00005 in the most extreme case), whereas all analyses that recover paraphyly indicate lack of significant incongruence. Numerous lines of evidence verify that monophyly is the accurate phylogenetic result. Therefore, this study contributes to a growing body of information affirming that measures of incongruence should not be used as indicators of data set combinability.     

Understanding phylogenetic incongruence: lessons from phyllostomid bats

All characters and trait systems in an organism share a common evolutionary history that can be estimated using phylogenetic methods. However, differential rates of change and the evolutionary mechanisms driving those rates result in pervasive phylogenetic conflict. These drivers need to be uncovered because mismatches between evolutionary processes and phylogenetic models can lead to high confidence in incorrect hypotheses. Incongruence between phylogenies derived from morphological versus molecular analyses, and between trees based on different subsets of molecular sequences has become pervasive as datasets have expanded rapidly in both characters and species. For more than a decade, evolutionary relationships among members of the New World bat family Phyllostomidae inferred from morphological and molecular data have been in conflict. Here, we develop and apply methods to minimize systematic biases, uncover the biological mechanisms underlying phylogenetic conflict, and outline data requirements for future phylogenomic and morphological data collection. We introduce new morphological data for phyllostomids and outgroups and expand previous molecular analyses to eliminate methodological sources of phylogenetic conflict such as taxonomic sampling, sparse character sampling, or use of different algorithms to estimate the phylogeny. We also evaluate the impact of biological sources of conflict: saturation in morphological changes and molecular substitutions, and other processes that result in incongruent trees, including convergent morphological and molecular evolution. Methodological sources of incongruence play some role in generating phylogenetic conflict, and are relatively easy to eliminate by matching taxa, collecting more characters, and applying the same algorithms to optimize phylogeny. The evolutionary patterns uncovered are consistent with multiple biological sources of conflict, including saturation in morphological and molecular changes, adaptive morphological convergence among nectar‐feeding lineages, and incongruent gene trees. Applying methods to account for nucleotide sequence saturation reduces, but does not completely eliminate, phylogenetic conflict. We ruled out paralogy, lateral gene transfer, and poor taxon sampling and outgroup choices among the processes leading to incongruent gene trees in phyllostomid bats. Uncovering and countering the possible effects of introgression and lineage sorting of ancestral polymorphism on gene trees will require great leaps in genomic and allelic sequencing in this species‐rich mammalian family. We also found evidence for adaptive molecular evolution leading to convergence in mitochondrial proteins among nectar‐feeding lineages. In conclusion, the biological processes that generate phylogenetic conflict are ubiquitous, and overcoming incongruence requires better models and more data than have been collected even in well‐studied organisms such as phyllostomid bats.     

EVOLUTION OF PAEDOMORPHOSIS IN PLETHODONTID SALAMANDERS: ECOLOGICAL CORRELATES AND RE‐EVOLUTION OF METAMORPHOSIS

Life‐history modes can profoundly impact the biology of a species, and a classic example is the dichotomy between metamorphic (biphasic) and paedomorphic (permanently aquatic) life‐history strategies in salamanders. However, despite centuries of research on this system, several basic questions about the evolution of paedomorphosis in salamanders have not been addressed. Here, we use a nearly comprehensive, time‐calibrated phylogeny of spelerpine plethodontids to reconstruct the evolution of paedomorphosis and to test if paedomorphosis is (1) reversible; (2) associated with living in caves; (3) associated with relatively dry climatic conditions on the surface; and (4) correlated with limited range size and geographic dispersal. We find that paedomorphosis arose multiple times in spelerpines. We also find evidence for re‐evolution of metamorphosis after several million years of paedomorphosis in a lineage of Eurycea from the Edwards Plateau region of Texas. We also show for the first time using phylogenetic comparative methods that paedomorphosis is highly correlated with cave‐dwelling, arid surface environments, and small geographic range sizes, providing insights into both the causes and consequences of this major life history transition.     

ARTIFICIAL SELECTION FOR PAEDOMORPHOSIS IN THE SALAMANDER AMBYSTOMA TALPOIDEUM

Heterochronic ontogenetic mechanisms such as paedomorphosis are potentially important mechanisms of both microevolutionary and macroevolutionary change. The salamander Ambystoma talpoideum is facultatively paedomorphic. Expression of paedomorphosis in this species varies among local natural populations. Two breeding lines, one from a population associated with a temporary pond where metamorphosis to a terrestrial adult always occurs, another from a population associated with a nearly permanent pond where paedomorphosis is common, were selected artificially for paedomorphosis over four generations. The F₅ generation of each breeding line was reared in a “common garden” field experiment under two drying regimes to simulate the larval environment in a temporary and in a permanent pond. There was a significantly different response to the drying regimes and to the artificial selection in the two lines. A significant population × selection interaction indicated that the two populations responded differently to artificial selection for paedomorphosis. The presence of heritable genetic variation suggests that evolution and divergence among populations of salamanders is possible with intense natural selection over short periods of ecological time.     

Corroboration among Data Sets in Simultaneous Analysis: Hidden Support for Phylogenetic Relationships among Higher Level Artiodactyl Taxa

In the taxonomic congruence approach to systematics, data sets are analyzed separately, and corroboration among data sets is indicated by replicated components in topologies derived from the separate analyses. By contrast, in the total evidence and conditional combination approaches, characters from different data sets are mixed in combined phylogenetic analyses. In optimal topologies derived from such simultaneous analyses, support for a particular node may be attributed to one, some, or all of the individual data sets. Partitioned branch support (PBS) is one technique for describing the distribution of character support and conflict among data sets in simultaneous analysis. PBS is analogous to branch support (BS), but recognizes hidden support and conflicts that emerge with the combination of characters from different data sets. For both BS and PBS, support for a particular node is interpreted as the difference in cost between optimal and suboptimal topologies. A different measure, the clade stability index (CSI), assesses the robustness of a particular node through the successive removal of characters. Here, we introduce variations of the CSI, the data set removal index (DRI) and nodal data set influence (NDI), that indicate the stability of a particular node to the removal of entire data sets. Like PBS, the DRI and NDI summarize the influence of different data sets in simultaneous analysis. However, because these new methods and PBS use different perturbations to assess stability, DRI and NDI scores do not always predict PBS scores and vice versa. In this report, the DRI and NDI are compared to PBS and taxonomic congruence in a cladistic analysis of 17 data sets for Artiodactyla (Mammalia). Five indices of hidden support and conflict are defined and applied to the combined artiodactyl character set. These measures identify substantial hidden support for controversial relationships within Artiodactyla. Hidden character support is ignored in the taxonomic congruence approach to systematics, but the DRI, NDI, and PBS utilize this cryptic information in estimates of support among data sets for a given node.     

Considering alternative life history modes and genetic divergence in conservation: a case study of the Oklahoma salamander

Alternative life history strategies can provide important variation for the long-term persistence of a lineage. However, conservation of such lineages can be complicated because each life history mode may have different habitat requirements and may be vulnerable to different environmental perturbations. The Oklahoma salamander (Eurycea tynerensis) is endemic to the Ozark Plateau of North America, and has two discrete life history modes, biphasic (metamorphic) and aquatic (paedomorphic). Until recently, these modes were considered separate species and conservation attention focused only on paedomorphic populations. We perform phylogenetic analyses of the mitochondrial gene cytochrome b (Cytb) and nuclear gene proopiomelanocortin (POMC) to assess patterns of historical isolation in E. tynerensis, and test whether life history mode is randomly distributed with respect to the phylogeny and geography. We find three divergent Cytb lineages and significant shifts in POMC allele frequencies between the eastern, western, and southwestern portions of the distribution. Life history mode varies extensively, but paedomorphosis is largely restricted to the widespread western clade. Therefore, the two most divergent and narrowly distributed clades (southwestern and eastern) were previously overlooked due to their metamorphic life history. Paedomorphosis has allowed E. tynerensis to drastically increase its niche breadth and distribution size. Nevertheless, metamorphosis is also an important attribute, and metamorphic populations are the ultimate source for paedomorphic evolution. Preservation of divergent genetic lineages, and regions that include adjacent habitat for both life history modes, may be the most effective way to maintain historical and adaptive variation and provide gateways for ongoing life history evolution.     

Influence of data conflict and molecular phylogeny of major clades in Cimicomorphan true bugs (Insecta: Hemiptera: Heteroptera)

Cimicomorpha, which consists of 16 families representing more than 19,400 species, is the largest infraorder in Heteroptera, Insecta. We present the first molecular phylogenetic investigation of family relationships of Cimicomorpha, including 46 taxa from 12 of 16 Cimicomorphan families. Three genes, with a total of 3277 bp of sequence data (nuclear 18S rDNA: 2022 bp, 28S rDNA: 755 bp, and mitochondrial 16S rDNA: 498 bp) were analyzed. Data partitions were analyzed separately and in combination, by employing ML (maximum likelihood), MP (maximum parsimony), and Bayesian methods. As saturation was detected in substitutions of 16S rDNA, influence of data conflict in combined analyses was further explored by three methods: the incongruence length difference (ILD) test, the partitioned Bremer support (PBS), and the partition addition bootstrap alteration approach (PABA). PBS and PABA approaches suggested that 16S rDNA was not very suitable for addressing relationships at this level in Cimicomorpha. Our results also supported the nabid-cimicoid lineage for Cimicoidea proposed by Schuh and Stys [Schuh, R.T., Stys, P., 1991. Phylogenetic analysis of Cimicomorphan family relationships (Heteroptera). J. NY Entomol. Soc. 99 (3), 298-350]. Data incongruence and the utility of the three genes were briefly discussed.     

Data incongruence and the problem of avian louse phylogeny

Smith, V. S., Page, R. D. M. & Johnson, K. P. (2004). Data incongruence and the problem of avian louse phylogeny. — Zoologica Scripta, 33 , 239 –259.
Recent studies based on different types of data (i.e. morphological and molecular) have supported conflicting phylogenies for the genera of avian feather lice (Ischnocera: Phthiraptera). We analyse new and published data from morphology and from mitochondrial (12S rRNA and COI) and nuclear (EF1-α) genes to explore the sources of this incongruence and explain these conflicts. Character convergence, multiple substitutions at high divergences, and ancient radiation over a short period of time have contributed to the problem of resolving louse phylogeny with the data currently available. We show that apparent incongruence between the molecular datasets is largely attributable to rate variation and nonstationarity of base composition. In contrast, highly significant character incongruence leads to topological incongruence between the molecular and morphological data. We consider ways in which biases in the sequence data could be misleading, using several maximum likelihood models and LogDet corrections. The hierarchical structure of the data is explored using likelihood mapping and SplitsTree methods. Ultimately, we concede there is strong discordance between the molecular and morphological data and apply the conditional combination approach in this case. We conclude that higher level phylogenetic relationships within avian Ischnocera remain extremely problematic. However, consensus between datasets is beginning to converge on a stable phylogeny for avian lice, at and below the familial rank.     

A priori assumptions about characters as a cause of incongruence between molecular and morphological hypotheses of primate interrelationships

When molecules and morphology produce incongruent hypotheses of primate interrelationships, the data are typically viewed as incompatible, and molecular hypotheses are often considered to be better indicators of phylogenetic history. However, it has been demonstrated that the choice of which taxa to include in cladistic analysis as well as assumptions about character weighting, character state transformation order, and outgroup choice all influence hypotheses of relationships and may positively influence tree topology, so that relationships between extant taxa are consistent with those found using molecular data. Thus, the source of incongruence between morphological and molecular trees may lie not in the morphological data themselves but in assumptions surrounding the ways characters evolve and their impact on cladistic analysis. In this study, we investigate the role that assumptions about character polarity and transformation order play in creating incongruence between primate phylogenies based on morphological data and those supported by multiple lines of molecular data. By releasing constraints imposed on published morphological analyses of primates from disparate clades and subjecting those data to parsimony analysis, we test the hypothesis that incongruence between morphology and molecules results from inherent flaws in morphological data. To quantify the difference between incongruent trees, we introduce a new method called branch slide distance (BSD). BSD mitigates many of the limitations attributed to other tree comparison methods, thus allowing for a more accurate measure of topological similarity. We find that releasing a priori constraints on character behavior often produces trees that are consistent with molecular trees. Case studies are presented that illustrate how congruence between molecules and unconstrained morphological data may provide insight into issues of polarity, transformation order, homology, and homoplasy.     

Mitochondrial DNA,morphology, and the phylogenetic relationships of Antarctic icefishes (Notothenioidei: Channichthyidae)

The Channichthyidae is a lineage of 16 species in the Notothenioidei, a clade of fishes that dominate Antarctic near-shore marine ecosystems with respect to both diversity and biomass. Among four published studies investigating channichthyid phylogeny, no two have produced the same tree topology, and no published study has investigated the degree of phylogenetic incongruence between existing molecular and morphological datasets. In this investigation we present an analysis of channichthyid phylogeny using complete gene sequences from two mitochondrial genes (ND2 and 16S) sampled from all recognized species in the clade. In addition, we have scored all 58 unique morphological characters used in three previous analyses of channichthyid phylogenetic relationships. Data partitions were analyzed separately to assess the amount of phylogenetic resolution provided by each dataset, and phylogenetic incongruence among data partitions was investigated using incongruence length difference (ILD) tests. We utilized a parsimony-based version of the Shimodaira-Hasegawa test to determine if alternative tree topologies are significantly different from trees resulting from maximum parsimony analysis of the combined partition dataset. Our results demonstrate that the greatest phylogenetic resolution is achieved when all molecular and morphological data partitions are combined into a single maximum parsimony analysis. Also, marginal to insignificant incongruence was detected among data partitions using the ILD. Maximum parsimony analysis of all data partitions combined results in a single tree, and is a unique hypothesis of phylogenetic relationships in the Channichthyidae. In particular, this hypothesis resolves the phylogenetic relationships of at least two species (Channichthys rhinoceratus and Chaenocephalus aceratus), for which there was no consensus among the previous phylogenetic hypotheses. The combined data partition dataset provides substantial statistical power to discriminate among alternative hypotheses of channichthyid relationships. These findings suggest the optimal strategy for investigating the phylogenetic relationships of channichthyids is one that uses all available phylogenetic data in analyses of combined data partitions.     

Performance of criteria for selecting evolutionary models in phylogenetics: a comprehensive study based on simulated datasets

Background  

Explicit evolutionary models are required in maximum-likelihood and Bayesian inference, the two methods that are overwhelmingly used in phylogenetic studies of DNA sequence data. Appropriate selection of nucleotide substitution models is important because the use of incorrect models can mislead phylogenetic inference. To better understand the performance of different model-selection criteria, we used 33,600 simulated data sets to analyse the accuracy, precision, dissimilarity, and biases of the hierarchical likelihood-ratio test, Akaike information criterion, Bayesian information criterion, and decision theory.     

Flies and congruence

Competing phylogenetic hypotheses have become the rule in modern systematics. While the problem of incongruence between character sets has become extremely acute due to the generation of molecular data, it is by no means specific to molecular and morphological comparisons. The role of the modern systematist is to interpret incongruence between character sets and to come to some conclusion regarding a phylogenetic hypothesis of the organisms in question. Two aspects of congruence analysis are examined using the Drosophilidae as an example. The first includes the quantification of congruence and the types of phylogenetic inference that can be made from such analyses. The second aspect concerns an examination of character evolution in order to identify characters and taxa that might be contributing to incongruence in phylogenetic analysis. © 1994 Wiley-Liss, Inc.     

Molecules and Morphology,Phylogenetics and Genetics

Various explanations can be offered for the incongruence between phylogenetic hypotheses resulting from morphological and molecular data sets. Of these, the possibility that incongruence may result from the mutation of major morphogenetic genes leading to dramatic morphological divergence unaccompanied by equivalent change of the phylogenetic marker molecule(s) used is discussed in detail. As evidence for this hypothesis, several examples for such incongruence are surveyed. It seems possible that in many cases the genetic basis of the morphological characters responsible for the incongruence found may be simple, and that the genes involved may be homologous to genes known from mutant systems. It is suggested that: 1. the systematic documentation of incongruence between molecular and morphological phylogenies may help to assess the frequency of evolutionary change through the mutation of major morphogenetic genes, and that 2. the identification of major morphological characters distinguishing closely related taxa with mutant phenotypes known from mutant systems eventually may allow an experimental approach to the problem of evolutionary change resulting from major genes. Natural taxa suspected to be the result of such processes could be changed morphologically through transformation with the relevant genes.     

Life history plasticity does not confer resilience to environmental change in the mole salamander (<Emphasis Type="Italic">Ambystoma talpoideum)</Emphasis>

Plasticity in life history strategies can be advantageous for species that occupy spatially or temporally variable environments. We examined how phenotypic plasticity influences responses of the mole salamander, Ambystoma talpoideum, to disturbance events at the St. Marks National Wildlife Refuge (SMNWR), FL, USA from 2009 to 2014. We observed periods of extensive drought early in the study, in contrast to high rainfall and expansive flooding events in later years. Flooding facilitated colonization of predatory fishes to isolated wetlands across the refuge. We employed multistate occupancy models to determine how this natural experiment influenced the occurrence of aquatic larvae and paedomorphic adults and what implications this may have for the population. We found that, in terms of occurrence, responses to environmental variation differed between larvae and paedomorphs, but plasticity (i.e. the ability to metamorphose rather than remain in aquatic environment) was not sufficient to buffer populations from declining as a result of environmental perturbations. Drought and fish presence negatively influenced occurrence dynamics of larval and paedomorphic mole salamanders and, consequently, contributed to observed short-term declines of this species. Overall occurrence of larval salamanders decreased from 0.611 in 2009 to 0.075 in 2014 and paedomorph occurrence decreased from 0.311 in 2009 to 0.121 in 2014. Although variation in selection pressures has likely maintained this polyphenism previously, our results suggest that continued changes in environmental variability and the persistence of fish in isolated wetlands could lead to a loss of paedomorphosis in the SMNWR population and, ultimately, impact regional persistence in the future.     

Phylogenetic incongruence among oncogenic genital alpha human papillomaviruses

The human papillomaviruses (HPVs) have long been thought to follow a monophyletic pattern of evolution with little if any evidence for recombination between genomes. On the basis of this model, both oncogenicity and tissue tropism appear to have evolved once. Still, no systematic statistical analyses have shown whether monophyly is the rule across all HPV open reading frames (ORFs). We conducted a taxonomic analysis of 59 mucosal/genital HPVs using whole-genome and sliding-window similarity measures; maximum-parsimony, neighbor-joining, and Bayesian phylogenetic analyses; and localized incongruence length difference (LILD) analyses. The algorithm for the LILD analyses localized incongruence by calculating the tree length differences between constrained and unconstrained nodes in a total-evidence tree across all HPV ORFs. The process allows statistical evaluation of every ORF/node pair in the total-evidence tree. The most significant incongruence was observed at the putative high-risk (i.e., cancer-associated) node, the common oncogenic ancestor for alpha HPV species 9 (e.g., HPV type 16 [HPV16]), 11, 7 (e.g., HPV18), 5, and 6. Although these groups share early-gene homology, including high degrees of similarity among E6 and E7, groups 9 and 11 diverge from groups 7, 5, and 6 with respect to L2 and L1. The HPV species groups primarily associated with cervical and anogenital cancers appear to follow two distinct evolutionary paths, one conferred by the early genes and another by the late genes. The incongruence in the genital HPV phylogeny could have occurred from an early recombination event, an ecological niche change, and/or asymmetric genome convergence driven by intense selection. These data indicate that the phylogeny of the oncogenic HPVs is complex and that their evolution may not be monophyletic across all genes.