Phylogenetic analysis of non-stereotyped behavioural sequences with a successive event-pairing method

A new method is proposed which uses transitions among acts in non-stereotyped behavioural sequences as phylogenetic characters. This method is derived from the event-pairing method designed for the phylogenetic study of developmental sequences and from ethological analyses of transition matrices. It is applied to study the phylogenetic relationships within a well-known group, the presocial Zetoborinae cockroaches. The analysis is carried out with three data sets: a behavioural data set with transitions among acts in behavioural dyadic sequences, together with morphological and molecular data sets. Non-stereotyped behaviour proved to be phylogenetically informative and to display low homoplasy. This new method opens an avenue for studying the evolution of behaviour in the framework of phylogenetic analysis, which was restricted until now to the study of stereotyped sequences and/or isolated features involved in courting or building activities.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 853–867.     

Phylogenetic perspective on ecological niche evolution in american blackbirds (Family Icteridae)

Analysis of ecological characters on phylogenetic frameworks has only recently appeared in the literature, with several studies addressing patterns of niche evolution, generally over relatively recent time frames. In the present study, we examined patterns of niche evolution for a broad radiation of American blackbird species (Family Icteridae), exploring more deeply into phylogenetic history. Within each of three major blackbird lineages, overlap of ecological niches in principal components analysis transformed environmental space varied from high to none. Comparative phylogenetic analyses of ecological niche characteristics showed a general pattern of niche conservatism over evolutionary time, with differing degrees of innovation among lineages. Although blackbird niches were evolutionarily plastic over differing periods of time, they diverged within a limited set of ecological possibilities, resulting in examples of niche convergence among extant blackbird species. Hence, an understanding of the patterns of ecological niche evolution on broad phylogenetic scales sets the stage for framing questions of evolutionary causation, historical biogeography, and ancestral ecological characteristics more appropriately.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 869–878.     

Adaptive modifications of carapace outlines in the Cytheroidea (Ostracoda: Crustacea)

Shell outlines of 202 extant cytheroidean ostracods were analysed in dorsal, lateral, and posterior views by elliptic Fourier analysis. The results obtained confirm that the exterior morphology is related to ecological factors as well as phylogenetic constraints. Phytal species living on tall seagrass and benthic species burrowing in sediments are characterized and differentiated from the species crawling on sediments by the presence of slender shells with tapered venters. With reference to reconstruction of ancestral state of outline traits on the molecular phylogeny, the hypothetical ancestor of cytheroidean ostracods is presumed to have had an average-shaped shell. Morphological plasticity of the shell outline was observed in many families. The phytal species living on tall seagrass appear to have evolved convergently with species from other habitats, acquiring slim shell outlines during the Cenozoic period. The present analysis also reveals the phylogenetic constraints on the morphological evolution of the Trachyleberididae in their adaptation to a burrowing habit.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 97 , 810–821.     

Decoding the ‘zeep’ complex: quantitative analysis of interspecific variation in the nocturnal flight calls of nine wood warbler species (Parulidae spp.)

ABSTRACT

The “zeep” complex consists of nine birds that produce nocturnal flight calls with similar acoustic features. Our inability to distinguish these calls inhibits the acoustic monitoring of these species. We test the hypothesis that flight calls of nine warblers in the “zeep” complex show sufficient acoustic differences to allow differentiation. We investigate divergence in these vocalizations by recording birds held for banding and collecting additional recordings from sound libraries. We used three approaches to compare calls between species: analysis of variance in acoustic properties, discriminant analysis of acoustic properties, and spectrographic cross-correlation. The first approach revealed five species that were different in one or more acoustic properties. The second approach revealed a level of assignment to the correct species (73%) that exceeded levels expected by chance (36%). The third approach revealed calls of seven species to be significantly more similar to conspecific calls than heterospecific calls. Our results suggest the calls of many members of the “zeep” complex exhibit species-specific differences in structure, which may allow differentiation of at least five “zeep” species based on call alone. We advocate for the combined use of these three approaches for the comparison of “zeep” calls in future flight call studies.     

Bone histological correlates of high-frequency flapping flight and body mass in the furculae of birds: a phylogenetic approach

A parsimony optimization of the presence of high-frequency flapping flight onto a phylogeny of 29 species of birds shows that this is a derived character state that has been acquired at least four independent times: by the last common ancestor of Alcidae, that of Podicipedidae, that of Anatidae, and that of Rallidae. Cineradiographic analysis has shown that the furculae of birds underwent extraordinary deformations during the wingbeat cycle. Cyclical deformations are known to produce microfractures in the bone tissue, which may be a stimulus for Haversian remodelling, a mechanism of resorption and reconstruction of bone tissue that may repair bone microdamage. In the present study, we performed a comparative analysis in a phylogenetic context to test the effect of the frequency of cyclical deformations and body mass on the rate of Haversian remodelling in the furculae of birds. A variation partitioning analysis showed that the type of flight (high-frequency flapping flight vs. other kinds of flight of lower wing beat frequency) and body mass explained a significant portion of Haversian bone density (the outcome of Haversian remodelling) and that the phylogeny also explained a significant part of this variation. This phylogenetic signal on Haversian bone density variation may be the outcome of phylogenetic signal on the proximate causes producing Haversian remodelling.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 729–738.     

Phylogeny, biogeography, and recurrent evolution of divergent bill types in the nectar-stealing flowerpiercers (Thraupini: Diglossa and Diglossopis)

Neotropical tanagers known as flowerpiercers ( Diglossa and Diglossopis ) have a novel feeding adaptation, comprising a downward curved hook on the maxilla that allows these species to obtain floral nectar without pollination. Using mitochondrial DNA sequences, the phylogenetic relationships of all 18 species of flowerpiercers were studied for the first time. Strong support was found for the monophyly of flowerpiercers and for the monophyly of four superspecies within flowerpiercers. However, previously described species-groups, as well as the genus Diglossopis , are not monophyletic. The biogeographic origin of flowerpiercers was identified as Andean, with a single dispersal event from the northern Andes to Central America and a single dispersal event from the northern Andes to the tepuis. The first principal component, representing a contrast between hook size and bill size, was mapped onto the phylogeny to examine the evolution of relative hook size in the group. Across the phylogeny, a relatively large hook and a relatively small hook evolved multiple times in unrelated lineages, indicating lability in bill morphology. Differences in hook size among sympatric species, together with habitat partitioning and behavioural differences, can explain the coexistence of multiple species of flowerpiercers at the same locality.   © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 14–28.     

Bat echolocation calls: adaptation and convergent evolution

Bat echolocation calls provide remarkable examples of 'good design' through evolution by natural selection. Theory developed from acoustics and sonar engineering permits a strong predictive basis for understanding echolocation performance. Call features, such as frequency, bandwidth, duration and pulse interval are all related to ecological niche. Recent technological breakthroughs have aided our understanding of adaptive aspects of call design in free-living bats. Stereo videogrammetry, laser scanning of habitat features and acoustic flight path tracking permit reconstruction of the flight paths of echolocating bats relative to obstacles and prey in nature. These methods show that echolocation calls are among the most intense airborne vocalizations produced by animals. Acoustic tracking has clarified how and why bats vary call structure in relation to flight speed. Bats using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localized accurately. Recent phylogenetic analyses based on gene sequences show that particular types of echolocation signals have evolved independently in several lineages of bats. Call design is often influenced more by perceptual challenges imposed by the environment than by phylogeny, and provides excellent examples of convergent evolution. Now that whole genome sequences of bats are imminent, understanding the functional genomics of echolocation will become a major challenge.     

Bioacoustic and genetic divergence in a frog with a wide geographical distribution

The study of intraspecific variation of acoustic signals and its relationship with genetic divergence is important for understanding the origin of divergence in communication systems. We studied geographical variation in the acoustic structure of advertisement calls from five populations of the four‐eyed frog, Pleurodema thaul, and its relationship with the genetic divergence among these populations. By analyzing temporal and spectral parameters of the advertisement calls, we report that the signals of northern, central, and southern populations have remarkable differences between them. A phylogeographical analysis from a mitochondrial DNA fragment demonstrated three phylogenetic groups coincident with those found with the bioacoustics analysis. Furthermore, bioacoustic and genetic distances show significant correlations after controlling for geographical distance. These results suggest that behavioural divergence among populations of P. thaul has a phylogenetic basis, supporting three evolutionary units within this species, as well as prompting the exploration of divergence processes in the sound communication system of this species. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 142–155.     

Neotropical frogs and mating songs: The evolution of advertisement calls in glassfrogs

Anurans emit advertisement calls with the purpose of attracting mates and repelling conspecific competitors. The evolution of call traits is expected to be associated with the evolution of anatomical and behavioural traits due to the physics of call emission and transmission. The evolution of vocalizations might imply trade‐offs with other energetically costly behaviours, such as parental care. Here, we investigated the association between body size, calling site, parental care and call properties (call duration, number of notes, peak frequency, frequency bandwidth and call structure) of the advertisement calls of glassfrogs (Centrolenidae)—a family of Neotropical, leaf‐dwelling anurans—using phylogenetic comparative methods. We also explored the tempo and mode of evolution of these traits and compared them with those of three morphological traits associated with body size, locomotion and feeding. We generated and compiled acoustic data for 72 glassfrog species (46% of total species richness), including representatives of all genera. We found that almost all acoustic traits have significant, but generally modest, phylogenetic signal. Peak frequency of calls is significantly associated with body size, whereas call structure is significantly associated with calling site and paternal care. Thus, the evolution of body size, calling site and paternal care could constrain call evolution. The estimated disparity of acoustic traits was larger than that of morphological traits and the peak in disparity of acoustic traits generally occurred later in the evolution of glassfrogs, indicating a historically recent outset of the acoustic divergence in this clade.     

A comprehensive phylogeny of the bumble bees (Bombus)

Bumble bees ( Bombus Latreille) occupy a wide diversity of habitats, from alpine meadows to lowland tropical forest, yet they appear to be similar in morphology throughout their range, suggesting that behavioural adaptations play a more important role in colonizing diverse habitats. Notwithstanding their structural homogeneity, bumble bees exhibit striking inter- and intraspecific variation in colour pattern, purportedly the outcome of mimetic evolution. A robust phylogeny of Bombus would provide the framework for elucidating the history of their wide biogeographical distribution and the evolution of behavioural and morphological adaptations, including colour pattern. However, morphological studies of bumble bees have discovered too few phylogenetically informative characters to reconstruct a robust phylogeny. Using DNA sequence data, we report the first nearly complete species phylogeny of bumble bees, including most of the 250 known species from the 38 currently recognized subgenera. Bayesian analysis of nuclear (opsin, EF-1α, arginine kinase, PEPCK) and mitochondrial (16S) sequences results in a highly resolved and strongly supported phylogeny from base to tips, with clear-cut support for monophyly of most of the conventional morphology-based subgenera. Most subgenera fall into two distinct clades ( short-faced and long-faced ) associated broadly with differences in head morphology. Within the short-faced clade is a diverse New World clade, which includes nearly one-quarter of the currently recognized subgenera, many of which are restricted to higher elevations of Central and South America. The comprehensive phylogeny provides a firm foundation for reclassification and for evaluating character evolution in the bumble bees.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 161–188.     

Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea)

The evolution and determinants of host specificity in Lamellodiscus species (Monogenea, Diplectanidae) were investigated. The 20 known Mediterranean species were studied, all parasites of fishes from the family Sparidae (Teleostei). An index of specificity, which takes into account the phylogenetic relationships of their fish host species, was defined. The link between specificity and its potential determinants was investigated in a phylogenetic context using the method of independent contrasts. Host specificity in Lamellodiscus species appeared to be highly constrained by phylogeny, but also linked to host size. Mapping specificity onto the parasite phylogenetic tree suggests that specialist species do not represent an evolutionary dead end, and that specialization is not a derived condition. It is hypothesized that the ability to be generalist or specialist in Lamellodiscus is controlled by intrinsic, phylogenetically-related characteristics, and that specialist species tend to use large hosts, which may be more predictable.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77, 431−443.     

Ecological diversification and phylogeny of emydid turtles

Ecological diversification is a central topic in ecology and evolutionary biology. We undertook the first comprehensive species-level phylogenetic analysis of Emydidae (an ecologically diverse group of turtles), and used the resulting phylogeny to test four general hypotheses about ecological diversification. Phylogenetic analyses were based on data from morphology (237 parsimony-informative characters) and mitochondrial DNA sequences (547 parsimony-informative characters) and included 39 of the 40 currently recognized emydid species. Combined analyses of all data provide a well-supported hypothesis for intergeneric relationships, and support monophyly of the two subfamilies (Emydinae and Deirochelyinae) and most genera (with the notable exception of Clemmys and Trachemys ). Habitat and diet were mapped onto the combined-data tree to test fundamental hypotheses about ecological diversification. Using continuous coding of ecological characters showed that lineages changed in habitat before diet, ecological change was most frequently from generalist to specialist, and habitat and diet rarely changed on the same branch of the phylogeny. However, we also demonstrate that the results of ancestral trait reconstructions can be highly sensitive to character coding method (i.e. continuous vs. discrete). Finally, we propose a simple model to describe the pattern of ecological diversification in emydid turtles and other lineages, which may reconcile the (seemingly) conflicting conclusions of our study and two recent reviews of ecological diversification.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79, 577–610.     

Snake diets and the deep history hypothesis

The structure of animal communities has long been of interest to ecologists. Two different hypotheses have been proposed to explain origins of ecological differences among species within present‐day communities. The competition–predation hypothesis states that species interactions drive the evolution of divergence in resource use and niche characteristics. This hypothesis predicts that ecological traits of coexisting species are independent of phylogeny and result from relatively recent species interactions. The deep history hypothesis suggests that divergences deep in the evolutionary history of organisms resulted in niche preferences that are maintained, for the most part, in species represented in present‐day assemblages. Consequently, ecological traits of coexisting species can be predicted based on phylogeny regardless of the community in which individual species presently reside. In the present study, we test the deep history hypothesis along one niche axis, diet, using snakes as our model clade of organisms. Almost 70% of the variation in snake diets is associated with seven major divergences in snake evolutionary history. We discuss these results in the light of relevant morphological, behavioural, and ecological correlates of dietary shifts in snakes. We also discuss the implications of our results with respect to the deep history hypothesis. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 476–486.     

Is the morphological disparity of lemur skulls (Primates) controlled by phylogeny and/or environmental constraints?

The cranial morphology of Lemur catta and of the five species of the genus Eulemur is investigated here by landmark identification and Procrustes superimpositions. This geometrical morphometric method makes it possible to describe pure shape differences independent of size effects, and to quantify differences between specimens. The aim of this study is to determine whether the morphological disparity of lemur skulls is constrained by the environment and/or by the group's phylogenetic history. First, Procrustes residuals are analysed by principal component analysis and the scatter-plots interpreted against the geographical distributions of taxa to determine whether morphology is correlated with geography. Then, a morphological distance tree is computed and compared with various cladograms reported in the literature to test for any correlation between morphology and phylogeny. Morphological disparity is found to be closely correlated with geographical distribution but independent of phylogeny. This confirms that the morphological disparity of lemur skulls is associated with a high degree of homoplasy, probably as a result of ecological constraints.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 577–590.     

Interspecific variation of acoustic signals in Mediterranean gobies (Perciformes, Gobiidae): comparative analysis and evolutionary outlook

Sound production of 11 Mediterranean goby species, belonging to five different genera, have been comparatively analysed on the basis of the quantitative properties of the acoustic signal emitted by the male in both the reproductive and aggressive context. The results obtained showed that three groups of species can be recognized on the basis of signal similarity: the larger sized species (genus Padogobius and Gobius paganellus ) producing tonal sounds, showing high values of pulse rate and low values of duration; the larger-sized species producing grunt sounds (genus Gobius and Zosterisessor ) with low pulse rate and low duration; and the small-sized species producing grunt sounds (genus Pomatoschistus and Knipowitschia ) with low pulse rate and high duration. The comparison between these results and those found in previous studies suggests congruence between the acoustic affinities among species and that obtained by means of morphological and genetic data. Furthermore, first hypotheses on the evolution of acoustic communication and the associated mechanisms in this fish group are suggested.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 763–778.     

Intraguild interactions promote assortative mating and affect sexual attractiveness in a phytophagous fly

Changes in acoustic and substrate-borne sexual signals in phytophagous insects associated with host plant shifts are known to have the potential to promote assortative mating, reproductive isolation and speciation. In this article, we ask whether the switch between pure herbivory and intraguild predation (IGP), which is common amongst phytophagous insects, has similar potential. Male flies in the genus Lipara (Diptera: Chloropidae) search for females by vibrating reed stems and waiting for a reply. By kleptoparasitizing other phytophagous species in the genus (a form of IGP), Lipara rufitarsis can increase its nonsexual fitness considerably. We looked at the impact of IGP on the timing of hatching, body size and attractiveness of male calls in L. rufitarsis . L. rufitarsis males that had engaged in IGP hatched significantly earlier than purely phytophagous flies and were significantly larger, but their calls were less likely to elicit responses from females during playback experiments. We conclude that, although behavioural observations of females provided no evidence of 'like preferring like', changes in phenology associated with IGP are likely to promote assortative mating in this system. The general preference of females for the calls of smaller males is a phenomenon worthy of further study: it may have no adaptive significance, or it may indicate that mating with large males is associated with a fitness cost.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 171–180.     

Phylogeny and species traits predict bird detectability

Avian acoustic communication has resulted from evolutionary pressures and ecological constraints. We therefore expect that auditory detectability in birds might be predictable by species traits and phylogenetic relatedness. We evaluated the relationship between phylogeny, species traits, and field‐based estimates of the two processes that determine species detectability (singing rate and detection distance) for 141 bird species breeding in boreal North America. We used phylogenetic mixed models and cross‐validation to compare the relative merits of using trait data only, phylogeny only, or the combination of both to predict detectability. We found a strong phylogenetic signal in both singing rates and detection distances; however the strength of phylogenetic effects was less than expected under Brownian motion evolution. The evolution of behavioural traits that determine singing rates was found to be more labile, leaving more room for species to evolve independently, whereas detection distance was mostly determined by anatomy (i.e. body size) and thus the laws of physics. Our findings can help in disentangling how complex ecological and evolutionary mechanisms have shaped different aspects of detectability in boreal birds. Such information can greatly inform single‐ and multi‐species models but more work is required to better understand how to best correct possible biases in phylogenetic diversity and other community metrics.     

Molecular phylogeny and phylogeography of the Greek populations of the genus Orthometopon (Isopoda, Oniscidea) based on mitochondrial DNA sequences

We infer phylogenetic relationships among isopod species of the genus Orthometopon distributed in the Greek area, comparing partial mitochondrial DNA sequences for cytochrome oxidase I (COI). All phylogenetic analyses produced topologically identical trees that revealed a well-resolved phylogeny. These trees support the monophyly of the genus Orthometopon , and suggest two clades that correspond to separate geographical regions (west and east of the mid-Aegean trench). However, the phylogenetic relationships among Greek populations of Orthometopon spp. are different from the presumed pattern on the basis of morphological evidence. The distinct geographical distribution of the major clades of the phylogenetic tree and its topology suggest a spatial and temporal sequence of phylogenetic separations, which coincide with some major palaeogeographical separations during the geological history of the Aegean Sea. The results stress the need for a reconsideration of the evolutionary history of Orthometopon species, which will help overcome difficulties encountered in classical taxonomy at the species level. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society , 2008, 152 , 707–715.     

Assessing the taxonomic status of tropical frogs through bioacoustics: geographical variation in the advertisement calls in the Eleutherodactylus discoidalis species group (Anura)

The taxonomic status of a very poorly known group of Andean frogs (the Eleutherodactylus discoidalis group) is assessed through acoustic and statistical analyses of differences in temporal parameters of advertisement calls, such as the number of pulses and the call duration, and also in a spectral parameter, dominant frequency. As these species are usually misidentified or ignored because of their taxonomic complexity in both ecological and biodiversity studies, we provide a bioacoustical diagnosis for each species in order to facilitate identification in the field. Differences in acoustic parameters support the specific status of Eleutherodactylus cruralis , E. discoidalis , Eleutherodactylus ibischi , and Eleutherodactylus madidi . The name E. cruralis is probably applied to three different species: the nominal form from Amazonian forests of the Andean slopes and adjacent lowlands, and two cryptic species restricted to inter-Andean dry valleys and cloud forests from central Bolivia. Moreover, the distribution of energy through the call and the aggregation of pulses seem to be useful meristic characters for detecting interspecific differences. Populations from each macrohabitat can be recognized by distinctive advertisement calls, usually corresponding to a recognized species. For the whole group, pulse rate is significantly correlated to latitude, which could indicate a speciation process along the Andes in relation to habitat changes and isolation. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society , 2008, 152 , 353–365.