Different profiles of soil phosphorous compounds depending on tree species and availability of soil phosphorus in a tropical rainforest in French Guiana.

BACKGROUND: The availability of soil phosphorus (P) often limits the productivities of wet tropical lowland forests. Little is known, however, about the metabolomic profile of different chemical P compounds with potentially different uses and about the cycling of P and their variability across space under different tree species in highly diverse tropical rainforests. RESULTS: We hypothesised that the different strategies of the competing tree species to retranslocate, mineralise, mobilise, and take up P from the soil would promote distinct soil 31P profiles. We tested this hypothesis by performing a metabolomic analysis of the soils in two rainforests in French Guiana using 31P nuclear magnetic resonance (NMR). We analysed 31P NMR chemical shifts in soil solutions of model P compounds, including inorganic phosphates, orthophosphate mono- and diesters, phosphonates, and organic polyphosphates. The identity of the tree species (growing above the soil samples) explained > 53% of the total variance of the 31P NMR metabolomic profiles of the soils, suggesting species-specific ecological niches and/or species-specific interactions with the soil microbiome and soil trophic web structure and functionality determining the use and production of P compounds. Differences at regional and topographic levels also explained some part of the the total variance of the 31P NMR profiles, although less than the influence of the tree species. Multivariate analyses of soil 31P NMR metabolomics data indicated higher soil concentrations of P biomolecules involved in the active use of P (nucleic acids and molecules involved with energy and anabolism) in soils with lower concentrations of total soil P and higher concentrations of P-storing biomolecules in soils with higher concentrations of total P. CONCLUSIONS: The results strongly suggest "niches" of soil P profiles associated with physical gradients, mostly topographic position, and with the specific distribution of species along this gradient, which is associated with species-specific strategies of soil P mineralisation, mobilisation, use, and uptake.

Weak warning signals can persist in the absence of gene flow.

Aposematic organisms couple conspicuous warning signals with a secondary defense to deter predators from attacking. Novel signals of aposematic prey are expected to be selected against due to positive frequency-dependent selection. How, then, can novel phenotypes persist after they arise, and why do so many aposematic species exhibit intrapopulation signal variability? Using a polytypic poison frog (Dendrobates tinctorius), we explored the forces of selection on variable aposematic signals using 2 phenotypically distinct (white, yellow) populations. Contrary to expectations, local phenotype was not always better protected compared to novel phenotypes in either population; in the white population, the novel phenotype evoked greater avoidance in natural predators. Despite having a lower quantity of alkaloids, the skin extracts from yellow frogs provoked higher aversive reactions by birds than white frogs in the laboratory, although both populations differed from controls. Similarly, predators learned to avoid the yellow signal faster than the white signal, and generalized their learned avoidance of yellow but not white. We propose that signals that are easily learned and broadly generalized can protect rare, novel signals, and weak warning signals (i.e., signals with poor efficacy and/or poor defense) can persist when gene flow among populations, as in this case, is limited. This provides a mechanism for the persistence of intrapopulation aposematic variation, a likely precursor to polytypism and driver of speciation.

Climatic breadth of calling behaviour in two widespread Neotropical frogs: Insights from humidity extremes.

Climate change is severely altering precipitation regimes at local and global scales, yet the capacity of species to cope with these changes has been insufficiently examined. Amphibians are globally endangered and particularly sensitive to moisture conditions. For mating, most amphibian species rely on calling behaviour, which is a key weather-dependent trait. Using passive acoustics, we monitored the calling behaviour of two widespread Neotropical frogs in 12 populations located at the humidity extremes but thermal mean of the species distribution. Based on 2,554 hr of recordings over a breeding season, we found that both the aquatic species Pseudis paradoxa and the arboreal species Boana raniceps exhibited calling behaviour at a wide range of relative humidity. Calling humidity was significantly lower in conspecific populations subjected to drier conditions, while calling temperature did not differ between populations or species. Overall, no variation in climatic breadth was observed between large and small choruses, and calling behaviour was scarcely detected during the driest, hottest and coldest potential periods of breeding. Our results showed that calling humidity of the studied species varies according to the precipitation regime, suggesting that widespread Neotropical anurans may have the capacity to exhibit sexual displays in different climatic environments. Regardless of the underlying mechanism (plasticity or local adaptation), which should be determined by common garden experiments, a wide and population-specific climatic breadth of calling behaviour may assist species to deal with changing humidity conditions. To our knowledge, this is the first study to explore the response capacity of anurans to perform calling behaviour under contrasting precipitation regimes.

31P-NMR Metabolomics Revealed Species-Specific Use of Phosphorous in Trees of a French Guiana Rainforest.

Productivity of tropical lowland moist forests is often limited by availability and functional allocation of phosphorus (P) that drives competition among tree species and becomes a key factor in determining forestall community diversity. We used non-target 31P-NMR metabolic profiling to study the foliar P-metabolism of trees of a French Guiana rainforest. The objective was to test the hypotheses that P-use is species-specific, and that species diversity relates to species P-use and concentrations of P-containing compounds, including inorganic phosphates, orthophosphate monoesters and diesters, phosphonates and organic polyphosphates. We found that tree species explained the 59% of variance in 31P-NMR metabolite profiling of leaves. A principal component analysis showed that tree species were separated along PC 1 and PC 2 of detected P-containing compounds, which represented a continuum going from high concentrations of metabolites related to non-active P and P-storage, low total P concentrations and high N:P ratios, to high concentrations of P-containing metabolites related to energy and anabolic metabolism, high total P concentrations and low N:P ratios. These results highlight the species-specific use of P and the existence of species-specific P-use niches that are driven by the distinct species-specific position in a continuum in the P-allocation from P-storage compounds to P-containing molecules related to energy and anabolic metabolism.

Nutrient scarcity strengthens soil fauna control over leaf litter decomposition in tropical rainforests.

Soil fauna is a key control of the decomposition rate of leaf litter, yet its interactions with litter quality and the soil environment remain elusive. We conducted a litter decomposition experiment across different topographic levels within the landscape replicated in two rainforest sites providing natural gradients in soil fertility to test the hypothesis that low nutrient availability in litter and soil increases the strength of fauna control over litter decomposition. We crossed these data with a large dataset of 44 variables characterizing the biotic and abiotic microenvironment of each sampling point and found that microbe-driven carbon (C) and nitrogen (N) losses from leaf litter were 10.1 and 17.9% lower, respectively, in the nutrient-poorest site, but this among-site difference was equalized when meso- and macrofauna had access to the litterbags. Further, on average, soil fauna enhanced the rate of litter decomposition by 22.6%, and this contribution consistently increased as nutrient availability in the microenvironment declined. Our results indicate that nutrient scarcity increases the importance of soil fauna on C and N cycling in tropical rainforests. Further, soil fauna is able to equalize differences in microbial decomposition potential, thus buffering to a remarkable extent nutrient shortages at an ecosystem level.

Phenotypic and life-history diversification in Amazonian frogs despite past introgressions.

The advent of genomics in phylogenetics and population genetics strengthened the perception that conflicts among gene trees are frequent and often due to introgression. However, hybridization occurs mostly among species that exhibit little phenotypic differentiation. A recent study delineating species in Anomaloglossus, a frog genus endemic to the Guiana Shield, identified an intriguing pattern in the A. baeobatrachus species complex. This complex occurs in French Guiana and Amapá (Brazil) and comprises two sympatric phenotypes contrasting not only in body size, habitat, and advertisement call, but also in larval development mode (endotrophic vs exotrophic tadpoles). However, molecular and phenotypic divergences are, in some cases, incongruent, i.e specimens sharing mtDNA haplotypes are phenotypically distinct, suggesting a complex evolutionary history. Therefore, we genotyped 106 Anomaloglossus individuals using ddRADseq to test whether this phenotype/genotype incongruence was a product of phenotypic plasticity, incomplete lineage sorting, multiple speciation events, or admixture. Based on more than 16,000 SNPs, phylogenetic and population genetic approaches demonstrated that exotrophic populations are paraphyletic. Species tree and admixture analyses revealed a strikingly reticulate pattern, suggesting multiple historical introgression events. The evolutionary history of one exotrophic population in northern French Guiana is particularly compelling given that it received genetic material from exotrophic ancestors but shows very strong genetic affinity with the nearby endotrophic populations. This suggests strong selection on larval development and mating call after secondary contact and hybridization. The case of A. baeobatrachus represents a striking example of introgression among lineages that are phenotypically distinct, even in their larval development mode, and highlights how high-resolution genomic data can unravel unexpectedly complex evolutionary scenarios.

Explosive breeding in tropical anurans: environmental triggers, community composition and acoustic structure.

BACKGROUND: Anurans largely rely on acoustic communication for sexual selection and reproduction. While multiple studies have focused on the calling activity patterns of prolonged breeding assemblages, species that concentrate their reproduction in short-time windows, explosive breeders, are still largely unknown, probably because of their ephemeral nature. In tropical regions, multiple species of explosive breeders may simultaneously aggregate leading to massive, mixed and dynamic choruses. To understand the environmental triggers, the phenology and composition of these choruses, we collected acoustic and environmental data at five ponds in French Guiana during a rainy season, assessing acoustic communities before and during explosive breeding events. RESULTS: We detected in each pond two explosive breeding events, lasting between 24 and 70 h. The rainfall during the previous 48 h was the most important factor predicting the emergence of these events. During explosive breeding events, we identified a temporal factor that clearly distinguished pre- and mid-explosive communities. A common pool of explosive breeders co-occurred in most of the events, namely Chiasmocleis shudikarensis, Trachycephalus coriaceus and Ceratophrys cornuta. Nevertheless, the species composition was remarkably variable between ponds and for each pond between the first and the second events. The acoustic structure of explosive breeding communities had outlying levels of amplitude and unexpected low acoustic diversity, significantly lower than the communities preceding explosive breeding events. CONCLUSIONS: Explosive breeding communities were tightly linked with specific rainfall patterns. With climate change increasing rainfall variability in tropical regions, such communities may experience significant shifts in their timing, distribution and composition. In structurally similar habitats, located in the same region without obvious barriers, our results highlight the variation in composition across explosive breeding events. The characteristic acoustic structure of explosive breeding events stands out from the circadian acoustic environment being easily detected at long distance, probably reflecting behavioural singularities and conveying heterospecific information announcing the availability of short-lived breeding sites. Our data provides a baseline against which future changes, possibly linked to climate change, can be measured, contributing to a better understanding on the causes, patterns and consequences of these unique assemblages.

Cryptic diversity in Amazonian frogs: Integrative taxonomy of the genus Anomaloglossus (Amphibia: Anura: Aromobatidae) reveals a unique case of diversification within the Guiana Shield.

Lack of resolution on species boundaries and distribution can hamper inferences in many fields of biology, notably biogeography and conservation biology. This is particularly true in megadiverse and under-surveyed regions such as Amazonia, where species richness remains vastly underestimated. Integrative approaches using a combination of phenotypic and molecular evidence have proved extremely successful in reducing knowledge gaps in species boundaries, especially in animal groups displaying high levels of cryptic diversity like amphibians. Here we combine molecular data (mitochondrial 16S rRNA and nuclear TYR, POMC, and RAG1) from 522 specimens of Anomaloglossus, a frog genus endemic to the Guiana Shield, including 16 of the 26 nominal species, with morphometrics, bioacoustics, tadpole development mode, and habitat use to evaluate species delineation in two lowlands species groups. Molecular data reveal the existence of 18 major mtDNA lineages among which only six correspond to described species. Combined with other lines of evidence, we confirm the existence of at least 12 Anomaloglossus species in the Guiana Shield lowlands. Anomaloglossus appears to be the only amphibian genus to have largely diversified within the eastern part of the Guiana Shield. Our results also reveal strikingly different phenotypic evolution among lineages. Within the A. degranvillei group, one subclade displays acoustic and morphological conservatism, while the second subclade displays less molecular divergence but clear phenotypic divergence. In the A. stepheni species group, a complex evolutionary diversification in tadpole development is observed, notably with two closely related lineages each displaying exotrophic and endotrophic tadpoles.

MSeasy: unsupervised and untargeted GC-MS data processing.

UNLABELLED: MSeasy performs unsupervised data mining on gas chromatography-mass spectrometry data. It detects putative compounds within complex metabolic mixtures through the clustering of mass spectra. Retention times or retention indices are used after clustering, together with other validation criteria, for quality control of putative compounds. The package generates a fingerprinting or profiling matrix compatible with NIST mass spectral search program and ARISTO webtool (Automatic Reduction of Ion Spectra To Ontology) for molecule identification. Most commonly used file formats, NetCDF, mzXML and ASCII, are acceptable. A graphical and user-friendly interface, MSeasyTkGUI, is available for R novices. AVAILABILITY: MSeasy and MSeasytkGUI are implemented as R packages available at http://cran.r-project.org/web/packages/MSeasy/index.html and http://cran.r-project.org/web/packages/MSeasyTkGUI/index.html.

A new species of the genus Pristimantis (Amphibia, Craugastoridae) associated with the moderately elevated massifs of French Guiana.

We describe a new Pristimantis from French Guiana, northern South America, which is mainly distinguished from known phenotypically related congeners (i.e. species from the polyphyletic unistrigatus species group) occurring at low and middle elevations in the Guiana Shield by the combination of a distinct tympanum, a lower ratio of tibia vs. hand length, a reddish groin region, and a distinct advertisement call consisting of clusters of generally four short notes. The new species inhabits pristine primary forests on the slopes of isolated massifs reaching more than 400 m elevation, and seems not to occur below ca. 200 m above sea level. Such a sharp altitudinal limit suggests a strong influence of thermal variation on the distribution of the species, and therefore a potential sensitivity to climate change. With only nine isolated populations documented so far, the new species should be prioritized for conservation. Historical climate fluctuations during the Quaternary are likely responsible for the distribution pattern of the new species. 

Foliar elementome and functional traits relationships identify tree species niche in French Guiana rainforests.

Biogeochemical niche (BN) hypothesis aims to relate species/genotype elemental composition with its niche based on the fact that different elements are involved differentially in distinct plant functions. We here test the BN hypothesis through the analysis of the 10 foliar elemental concentrations and 20 functional-morphological of 60 tree species in a French Guiana tropical forest. We observed strong legacy (phylogenic + species) signals in the species-specific foliar elemental composition (elementome) and, for the first time, provide empirical evidence for a relationship between species-specific foliar elementome and functional traits. Our study thus supports the BN hypothesis and confirms the general niche segregation process through which the species-specific use of bio-elements drives the high levels of α-diversity in this tropical forest. We show that the simple analysis of foliar elementomes may be used to test for BNs of co-occurring species in highly diverse ecosystems, such as tropical rainforests. Although cause and effect mechanisms of leaf functional and morphological traits in species-specific use of bio-elements require confirmation, we posit the hypothesis that divergences in functional-morphological niches and species-specific biogeochemical use are likely to have co-evolved.

Decay of similarity across tropical forest communities: integrating spatial distance with soil nutrients.

Understanding the mechanisms that drive the change of biotic assemblages over space and time is the main quest of community ecology. Assessing the relative importance of dispersal and environmental species selection in a range of organismic sizes and motilities has been a fruitful strategy. A consensus for whether spatial and environmental distances operate similarly across spatial scales and taxa, however, has yet to emerge. We used censuses of four major groups of organisms (soil bacteria, fungi, ground insects, and trees) at two observation scales (1-m2 sampling point vs. 2,500-m2 plots) in a topographically standardized sampling design replicated in two tropical rainforests with contrasting relationships between spatial distance and nutrient availability. We modeled the decay of assemblage similarity for each taxon set and site to assess the relative contributions of spatial distance and nutrient availability distance. Then, we evaluated the potentially structuring effect of tree composition over all other taxa. The similarity of nutrient content in the litter and topsoil had a stronger and more consistent selective effect than did dispersal limitation, particularly for bacteria, fungi, and trees at the plot level. Ground insects, the only group assessed with the capacity of active dispersal, had the highest species turnover and the flattest nonsignificant distance-decay relationship, suggesting that neither dispersal limitation nor nutrient availability were fundamental drivers of their community assembly at this scale of analysis. Only the fungal communities at one of our study sites were clearly coordinated with tree composition. The spatial distance at the smallest scale was more important than nutrient selection for the bacteria, fungi, and insects. The lower initial similarity and the moderate variation in composition identified by these distance-decay models, however, suggested that the effects of stochastic sampling were important at this smaller spatial scale. Our results highlight the importance of nutrients as one of the main environmental drivers of rainforest communities irrespective of organismic or propagule size and how the overriding effect of the analytical scale influences the interpretation, leading to the perception of greater importance of dispersal limitation and ecological drift over selection associated with environmental niches at decreasing observation scales.

Resistance and resilience of soil prokaryotic communities in response to prolonged drought in a tropical forest.

Global climate changes such as prolonged duration and intensity of drought can lead to adverse ecological consequences in forests. Currently little is known about soil microbial community responses to such drought regimes in tropical forests. In this study, we examined the resistance and resilience of topsoil prokaryotic communities to a prolongation of the dry season in terms of diversity, community structure and co-occurrence patterns in a French Guianan tropical forest. Through excluding rainfall during and after the dry season, a simulated prolongation of the dry season by five months was compared to controls. Our results show that prokaryotic communities increasingly diverged from controls with the progression of rain exclusion. Furthermore, prolonged drought significantly affected microbial co-occurrence networks. However, both the composition and co-occurrence networks of soil prokaryotic communities immediately ceased to differ from controls when precipitation throughfall returned. This study thus suggests modest resistance but high resilience of microbial communities to a prolonged drought in tropical rainforest soils.

High foliar K and P resorption efficiencies in old-growth tropical forests growing on nutrient-poor soils.

Resorption is the active withdrawal of nutrients before leaf abscission. This mechanism represents an important strategy to maintain efficient nutrient cycling; however, resorption is poorly characterized in old-growth tropical forests growing in nutrient-poor soils. We investigated nutrient resorption from leaves in 39 tree species in two tropical forests on the Guiana Shield, French Guiana, to investigate whether resorption efficiencies varied with soil nutrient, seasonality, and species traits. The stocks of P in leaves, litter, and soil were low at both sites, indicating potential P limitation of the forests. Accordingly, mean resorption efficiencies were higher for P (35.9%) and potassium (K; 44.6%) than for nitrogen (N; 10.3%). K resorption was higher in the wet (70.2%) than in the dry (41.7%) season. P resorption increased slightly with decreasing total soil P; and N and P resorptions were positively related to their foliar concentrations. We conclude that nutrient resorption is a key plant nutrition strategy in these old-growth tropical forests, that trees with high foliar nutrient concentration reabsorb more nutrient, and that nutrients resorption in leaves, except P, are quite decoupled from nutrients in the soil. Seasonality and biochemical limitation played a role in the resorption of nutrients in leaves, but species-specific requirements obscured general tendencies at stand and ecosystem level.

Different "metabolomic niches" of the highly diverse tree species of the French Guiana rainforests.

Tropical rainforests harbor a particularly high plant diversity. We hypothesize that potential causes underlying this high diversity should be linked to distinct overall functionality (defense and growth allocation, anti-stress mechanisms, reproduction) among the different sympatric taxa. In this study we tested the hypothesis of the existence of a metabolomic niche related to a species-specific differential use and allocation of metabolites. We tested this hypothesis by comparing leaf metabolomic profiles of 54 species in two rainforests of French Guiana. Species identity explained most of the variation in the metabolome, with a species-specific metabolomic profile across dry and wet seasons. In addition to this "homeostatic" species-specific metabolomic profile significantly linked to phylogenetic distances, also part of the variance (flexibility) of the metabolomic profile was explained by season within a single species. Our results support the hypothesis of the high diversity in tropical forest being related to a species-specific metabolomic niche and highlight ecometabolomics as a tool to identify this species functional diversity related and consistent with the ecological niche theory.

Diversity of the volatile organic compounds emitted by 55 species of tropical trees: a survey in French Guiana.

Volatile organic compounds (VOCs) are produced by a broad range of organisms, from bacteria to mammals, and they represent a vast chemical diversity. In plants, one of the preeminent roles of VOCs is their repellent or cytotoxic activity, which helps the plant deter its predators. Most studies on VOCs emitted by vegetative parts have been conducted in model plant species, and little is known about patterns of VOC emissions in diverse plant communities. We conducted a survey of the VOCs released immediately after mechanical damage of the bark and the leaves of 195 individual trees belonging to 55 tropical tree species in a lowland rainforest of French Guiana. We discovered a remarkably high chemical diversity, with 264 distinct VOCs and a mean of 37 compounds per species. Two monoterpenes (alpha-pinene and limonene) and two sesquiterpenes (beta-caryophyllene and alpha-copaene), which are known to have cytotoxic and deterrent effects, were the most frequent compounds in the sampled species. As has been established for floral scents, the blend of VOCs is largely species-specific and could be used to discriminate among 43 of the 55 sampled species. The species with the most diverse blends were found in the Sapindales, Laurales, and Magnoliales, indicating that VOC diversity is not uniformly distributed among tropical species. Interspecific variation in chemical diversity was caused mostly by variation in sesquiterpenes. This study emphasizes three aspects of VOC emission by tropical tree species: the species-specificity of the mixtures, the importance of sesquiterpenes, and the wide-ranging complexity of the mixtures.

A new species of Anomaloglossus (Anura: Aromobatidae) of the stepheni group with the redescription of A. baeobatrachus (Boistel and de Massary, 1999), and an amended definition of A. leopardus Ouboter and Jairam, 2012.

Anomaloglossus is a species-rich genus of frogs endemic to the Guiana Shield that still harbors several unnamed species. Within the A. stepheni species group (which includes four valid nominal species), A. baeobatrachus has an uncertain taxonomic status, notably because the holotype was an unvouchered specimen depicted in a popular journal. Another member of this group, A. leopardus, was only superficially described, lacking information on the sex of specimens in the type series and on advertisement call. Therefore, these two taxa need clarifications in order to allow the description of the extant undescribed species. In this paper, we redescribe A. baeobatrachus based on newly collected material from the species type locality and provide information about its reproductive ecology. We also provide an amended definition of A. leopardus using newly collected material from its type locality. These two species form a clade along with a third species from the Eastern Guiana Shield, which is also described herein. The reproductive biology of A. baeobatrachus and A. stepheni is very similar. Both species have endotrophic and nidicolous tadpoles, despite being distantly related, suggesting independent evolution of this breeding mode. The new species and A. leopardus, on the other hand, have exotrophic tadpoles.

On the brink of extinction: two new species of Anomaloglossus from French Guiana and amended definitions of Anomaloglossus degranvillei and A. surinamensis (Anura: Aromobatidae).

A large portion of the amphibian species occurring in Amazonia remains undescribed. A recent study on species delineation in Anomaloglossus, a genus endemic to the Guiana Shield, demonstrated the existence of two undescribed species previously identified as A. degranvillei, which we describe herein. In addition to divergence at the molecular level, these two new taxa are also distinguished by subtle morphological characters and substantial differences in the advertisement calls (note length, dominant frequency, note structure). One species occurs in the hilly lowlands of north-eastern French Guiana and is mainly distinguished from its closest relatives by a small body size (15.9-18.8 mm in males) and by vocalisations characterized by the emission of short notes of 0.09 s on average. The other species is only known from the Itoupé Massif in southern French Guiana and is mainly distinguished from its closest relatives by a moderate body size (19.4-20.4 mm in males) and by vocalisations characterized by the emission of long notes of 0.23 s on average. We also provide amended definitions for two previously described species in the A. degranvillei species group: A. degranvillei, which is endemic to a few massifs in central French Guiana, and A. surinamensis, which is distributed throughout Suriname and French Guiana. The new species described here and A. degranvillei have very narrow ranges within French Guiana and seem to have rapidly declined during the last decade. Therefore, we suggest A. degranvillei and A. dewynteri to be considered as "Critically Endangered" and A. blanci as "Vulnerable" according to the IUCN standards.

Recent Asian origin of chytrid fungi causing global amphibian declines.

Globalized infectious diseases are causing species declines worldwide, but their source often remains elusive. We used whole-genome sequencing to solve the spatiotemporal origins of the most devastating panzootic to date, caused by the fungus Batrachochytrium dendrobatidis, a proximate driver of global amphibian declines. We traced the source of B. dendrobatidis to the Korean peninsula, where one lineage, BdASIA-1, exhibits the genetic hallmarks of an ancestral population that seeded the panzootic. We date the emergence of this pathogen to the early 20th century, coinciding with the global expansion of commercial trade in amphibians, and we show that intercontinental transmission is ongoing. Our findings point to East Asia as a geographic hotspot for B. dendrobatidis biodiversity and the original source of these lineages that now parasitize amphibians worldwide.

Evolution of Sex-Biased Dispersal.

Dispersal is central in ecology and evolution because it influences population regulation, adaptation, and speciation. In many species, dispersal is different between genders, leading to sex-biased dispersal. Several theoretical hypotheses have been proposed to explain the evolution of this bias: the resource competition hypothesis proposed by Greenwood, the local mate competition hypothesis, and the inbreeding avoidance hypothesis. Those hypotheses argued that the mating system should be the major factor explaining the direction of such bias. Sociality and the presence of handicap in genders (exaggerated sexual characters or parental care) have recently been proposed to be linked with the direction of this bias. We tested these expected coevolutions using a database of 257 species. Based on phylogenetic approaches, our findings marginally corroborated Greenwood's hypothesis by showing relationships between the direction of sex-biased dispersal, mating systems, and territoriality. More importantly, our results highlighted that the evolution of this bias was more linked to parental care and sexual dimorphism. These traits were also found to be associated with mating systems, suggesting that sexual asymmetry in morphology and parental care might be the main determinant of the evolution of sex-biased dispersal across species and not mating systems per se, as proposed in Greenwood's hypothesis.