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Hierarchical decision‐making balances current and future reproductive success
research-article
Author(s):
Eva Ringler
1
,
2
,
3
,
,
Georgine Szipl
4 ,
Ryan J. Harrigan
5 ,
Perta Bartl‐Binder
3 ,
Rosanna Mangione
3
,
6 ,
Max Ringler
3
,
7
Publication date (Electronic):
23 April 2018
Journal:
Molecular Ecology
Publisher:
John Wiley and Sons Inc.
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Abstract
Parental decisions in animals are often context‐dependent and shaped by fitness trade‐offs between parents and offspring. For example, the selection of breeding habitats can considerably impact the fitness of both offspring and parents, and therefore, parents should carefully weigh the costs and benefits of available options for their current and future reproductive success. Here, we show that resource‐use preferences are shaped by a trade‐off between parental effort and offspring safety in a tadpole‐transporting frog. In a large‐scale in situ experiment, we investigated decision strategies across an entire population of poison frogs that distribute their tadpoles across multiple water bodies. Pool use followed a dynamic and sequential selection process, and transportation became more efficient over time. Our results point to a complex suite of environmental variables that are considered during offspring deposition, which necessitates a highly dynamic and flexible decision‐making process in tadpole‐transporting frogs.
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Most cited references52
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COLONY: a program for parentage and sibship inference from multilocus genotype data.
Owen R. Jones, Jinliang Wang (2010)
Pedigrees, depicting genealogical relationships between individuals, are important in several research areas. Molecular markers allow inference of pedigrees in wild species where relationship information is impossible to collect by observation. Marker data are analysed statistically using methods based on Mendelian inheritance rules. There are numerous computer programs available to conduct pedigree analysis, but most software is inflexible, both in terms of assumptions and data requirements. Most methods only accommodate monogamous diploid species using codominant markers without genotyping error. In addition, most commonly used methods use pairwise comparisons rather than a full-pedigree likelihood approach, which considers the likelihood of the entire pedigree structure and allows the simultaneous inference of parentage and sibship. Here, we describe colony, a computer program implementing full-pedigree likelihood methods to simultaneously infer sibship and parentage among individuals using multilocus genotype data. colony can be used for both diploid and haplodiploid species; it can use dominant and codominant markers, and can accommodate, and estimate, genotyping error at each locus. In addition, colony can carry out these inferences for both monoecious and dioecious species. The program is available as a Microsoft Windows version, which includes a graphical user interface, and a Macintosh version, which uses an R-based interface. © 2009 Blackwell Publishing Ltd.
- Record: found
- Abstract: not found
- Article: not found
Size and Timing of Metamorphosis in Complex Life Cycles: Time Constraints and Variation
Donald Ludwig, Locke Rowe (1991)
- Record: found
- Abstract: found
- Article: not found
Amazonian Amphibian Diversity Is Primarily Derived from Late Miocene Andean Lineages
Introduction Tropical regions contain more than half of biological diversity on just 7% of the Earth's surface [1,2]. Differences in biodiversity between tropical and temperate regions have been attributed to contrasting speciation and extinction rates [3]. Within the Neotropical realm, the Amazon Basin and the Chocoan region contain half of Earth's remaining rainforests and one of the largest reservoirs of terrestrial biodiversity. However, the impact of pre-Quaternary ecogeographic constraints on Neotropical biodiversity is largely unknown and the mechanisms contributing to species richness are unclear [3,4]. For example, the well-documented high α−diversity (species richness) of the flora and fauna of the Amazon rainforest [5] is usually attributed to local geoclimatic dynamics that promote monotonic accumulation of lineages [6,7]. However, the lower β−diversity (species turnover relative to distance) within the Amazon Basin is puzzling [8] and vastly underestimated. Current hypotheses are based on restricted, mostly Quaternary, spatiotemporal scales involving paleogeographic or ecological events (e.g., riverine barriers, Pleistocene climate change) [3], persistence of conservative niches [9], and analyses of phylogeography and endemicity [10]. In addition to speciation/extinction processes [3], major paleogeological events promote diversification, yielding complex phylogenetic patterns of vicariance, dispersal, and secondary sympatry [6]. Using phylogeographic analyses of the endemic and diverse clade of poison frogs (Dendrobatidae), we reconstructed Neotropical biogeography from the Oligocene to the present and revealed a widespread and highly dynamic pattern of multiple dispersals and radiations during the Miocene. Major geoclimatic events have shaped the Neotropics. The most important include the isolation and reconnection of South America, the uplift of the Andes, the extensive floodbasin system in the Amazonian Miocene, the formation of Orinoco and Amazon drainages, and the dry−wet climate cycles of the Pliocene−Pleistocene (Figure 1). The Panamanian Land Bridge (PLB) between the Chocó and Central America, which formed progressively until the Pliocene [11], was an important biogeographic catalyst of dispersal and vicariance events at the Miocene−Pliocene boundary (e.g., Alpheus shrimps and freshwater teleost fishes) [12,13]. Similarly, the uplift of the Andes advanced the formation of the Amazon River, converting a widespread, northwest-flowing Miocene floodbasin into the current eastward-running Amazon Basin [14,15]. Two Miocene marine incursions into this wetland system isolated several aquatic taxa as living relicts, including the Amazon River dolphin, lineages of marine-derived teleosts and stingrays, and brackish water mollusks [16,17]. However, controversies exist about the magnitude and duration of these geoclimatic events [18]. Figure 1 Biogeographic Areas, Extension of the Floodbasin System or Marine Incursions (Hatched Arrows), and Possible Connections within Cenozoic Paleogeographic Maps of Central and South America, Modified after Hoorn et al. and Diaz de Gamero (A–D) correspond to paleogeographic reconstruction of northern South America. (A) Early to late Eocene; (B) late Oligocene to middle Miocene; (C) middle to late Miocene; and (D) early Pliocene to the present. Uncertainties about the limit between biogeographic regions before the Pliocene are indicated by “?”. The hypotheses about the spatial configuration of biogeographic areas on the origin of Neotropical diversity are indicated in the panels (E–G) (input hypothesis matrices are provided in Figure S6). (E) The null model (H0: SM0), which assumes no spatial structure and equal rates of dispersal among all areas; (F) the center-of-origin model (HA: SM1), which assumes the Amazonia as the primary center of origin with widespread ancestral ranges constrained to include the Amazon Basin; and (G) the stepping-stone model (HA: SM2), which the assumes the historical spatial arrangement of biogeographic areas and constrains dispersals among geographically adjacent areas. The biogeographic areas used in the DEC modeling are C, the Amazon Basin; B, Guiana Shield; D, Venezuelan Highlands and Trinidad and Tobago Islands; E, North Oriental Andes; F, North Occidental Andes; G, Central Oriental Andes; and H, Central Occidental Andes; I, Chocoan rainforest, Magdalena Valley, and Gorgona Island; J, Central America west of the Gatun Fault Zone in Panamá; and K, the Brazilian Shield [14, 90]. Although well known for its megadiversity, no studies of the Neotropics have examined diversification patterns in highly speciose and widespread lineages over broad temporal and spatial scales. A general explanation that associates rates of speciation with paleogeographic events is lacking. Here, we test two general hypotheses about the spatial configuration of biogeographic areas on the origin of Neotropical diversity (Figure 1). First, under the center-of-origin hypothesis, lineages from the currently most diverse area (i.e., Amazon Basin) dispersed to other areas (Figure 1, HA: SM1). Second, under the stepping-stone hypothesis, paleogeographic events constrained the patterns of lineage diversification in the Neotropics among geographically adjacent areas (Figure 1, HA: SM2). Using a recently developed maximum likelihood (ML) procedure that estimates geographic range evolution, we tested both hypotheses against a null biogeographic model (Figure 1 H0: SM0) using a well-sampled Neotropical clade, the poison frogs (Dendrobatidae). We sampled 223 of the ∼353 (264 described and 34–89 undescribed) species, distributed from Central America and Guiana Shield to southeast Brazil and from Andean páramos (4,000 meters above sea level [masl]) to lowland rainforests ( 0.05). The nonsignificant comparison of SM2 and SM0 for the chronogram alone is likely due to its reduced taxon sample. The chronogram and a summary of the significant biogeographic events with confidence limits (Tables S8, S9A, and S9B) from the stepping-stone model are superimposed on the four major clades (Figure 2). The most recent ancestor of Dendrobatidae was distributed in regions that correspond to the current Venezuelan Highlands and Northern Oriental Andes at 40.9 ± 5.4 million years ago (MYA). This ancestral range split into a Venezuelan Highlands ancestor of clade A and an Andean ancestor (clade B + C + D). The most recent ancestor of each major clade occurred during the Oligocene at 34.9 ± 5.4 MYA (clade A), 30.9 ± 3.9 MYA (clade B), 27.1 ± 3.2 MYA (clade C), and 29.9 ± 4.0 MYA (clade D). We inferred 14 dispersals into and 18 from the Amazon Basin to adjacent areas, including three major radiations and a single lineage extinction within Amazonia. We also found five cross-Andean dispersals, five dispersals from Northern to Central Andes, six dispersals from Northern Andes to Chocó, four dispersals from Chocó to the Andes, and three temporal phases of lineage dispersal with two interleaved periods of vicariant events between the Chocó and Central America (Figure 2 and Table S12). The diversity of Amazonian poison frogs (>70 species) resulted from 14 separate dispersals into this region, in three phases (Figure 2). First, the two oldest dispersals originated independently from the Guiana Shield (23.8 MYA) and from the developing Andes (21.1 MYA), just before and during the existence of the Amazonian Miocene floodbasin. Second, a single dispersal from the Guiana Shield occurred 15.5 MYA, during a low sea-level period associated with reduction of the Miocene floodbasin system. Third, the 11 remaining dispersals from the Andes took place between (1.6–7.3 MYA) during the formation of the modern Amazon Basin river system. Ancestral area reconstructions using a Bayesian multistate procedure similarly support the recent multiple dispersals to the Amazon Basin (Figure 2). Thus, our results suggest that much of the extant Amazonian biodiversity results from relatively recent immigration of distinct lineages followed by in situ radiation during the last 10 MYA. At least 18 dispersals from the Amazon Basin to other areas were found in three temporal phases. First, the earliest dispersals to the developing Chocoan lowlands (21.8 MYA) and the Andes (15.2 MYA) occurred during the establishment of the Miocene floodbasin system. Interestingly, for the present Chocoan lineage of Dendrobates pumilio (Figure 2), our results suggest a Miocene overwater dispersal from Chocó to the developing Central America archipelago and the extinction of the Amazonian lineage ancestor at ∼19.5 MYA during the formation of the Miocene floodbasin system. Second, dispersals to the Guiana Shield (1), the Venezuela Highlands (1), and the Andes (1) took place after the Miocene floodbasin system receded (8.8–10.8 MYA). Third, the 12 remaining dispersals were very recent (0.7–6.0 MYA), to the Guiana Shield (7), Andes (4), and Brazilian Shield (1). Thus, 16 out of 18 occurred 40) also show a complex pattern of diversification at the end of the Miocene. Ten dispersals from Chocó to Central America suggest a pattern of recurrent colonization and isolation in three phases (Figure 2). First, the two oldest dispersals (8.3–12.1 MYA) from the Chocó overlap with a proposed earlier exchange of faunas during the late Miocene [29]. A single vicariant event at 6.8 MYA isolated the first wave of immigrants (i.e., ancestors of Phyllobates and Colostethus 1). Interestingly, the contemporaneous divergence of the Trinidad and Tobago species (Mannophryne trinitatis and M. olmonae) from Venezuelan relatives at 8.3 MYA suggests a global period of high sea level. Second, six Pliocene dispersals from South America (3.2–5.4 MYA), immediately followed a proposed low sea-level period after 6.0 MYA [11]. Six vicariant events in the middle Pliocene (1.1–3.6 MYA) are concomitant with a second high sea-level period (1.5–3.0 MYA) that separated Central America from the Chocó [11]. Third, two dispersals in the late Pleistocene (0.5–2.2 MYA) are contemporaneous with the Great Faunal Interchange at 1.2 MYA [11]. Likewise, the endemic poison frog of Gorgona Island (Epipedobates boulengeri), located 50 km off the Pacific coast, was derived from a Chocoan ancestor 2.4 MYA during the same period. Our results strongly support the repeated dispersal of poison frogs into Central America across the PLB before its final Pliocene closure. Similar results for the ancestral area reconstruction were obtained by dispersal-vicariance analysis (DIVA) [30]. However, DIVA provided unrealistic ancestral reconstructions for basal nodes (Figure S7), and a large number (i.e., ∼16 × 106) of equally parsimonious reconstructions (see Material and Methods). Therefore, DIVA analyses were considered exploratory due to its algorithmic limitations [26,31]. Lineage Diversification We estimated diversification rates of the chronogram (i.e., dendrobatid family clade) using the adjusted γ statistic to account for incomplete taxon sampling [32,33]. The γ statistic compares the relative position of the nodes in a chronogram to that expected under the pure birth model, and different values of γ characterize whether the diversification rate has increased (γ > 0), decreased (γ 2,000 m above sea level) [27] formed a significant barrier to dispersal, because no other cross-Andean dispersals were found. The uplift also was associated with dramatic ecological changes [27] and a decrease in diversification rates. These results suggest a role for niche conservatism [41,42], in that some lineages may have gone extinct because of failure to adapt. Alternatively, despite greater sampling effort in the Andes region than in other areas, we failed to find some previously common Andean species (e.g., Hyloxalus jacobuspetersi and the Ecuadorian H. lehmanni). Consequently, it is difficult to separate a natural decrease in diversification rates from the current trend of amphibian species extinctions at high altitudes due to anthropogenic habitat alteration [43], increased UV radiation [44], climate change [45], or pandemic infection [46]. In contrast, the montane transition zones of the Andes and adjacent lowlands (Chocó and Amazonia) have become centers of rapid cladogenesis (pattern 3), and species richness in these transition zones might be underestimated because many Neotropical lineages have been shown to contain several cryptic species [47]. Therefore, dispersals within or across the Andes diminished during the Pliocene, but diversification has intensified in the Andes-lowlands interface. Although some of the oldest lineages of poison frogs originated in the Guiana Shield and the Venezuelan Highlands (>30 species), our results suggest extended in situ diversification (pattern 2) followed by a decline in the rate of diversification of endemic clades in both areas since the early Miocene. Along the same lines, the Guiana Shield has high poison frog endemism, which is mostly restricted to the summits of the sandstone tepuis [48], while recent Amazonian poison frog immigrants occupy lowlands adjacent to the tepuis. Our results suggest that the decline of endemic Guianan diversity might be associated with ecological changes in habitat due to the collapse of the ancient tepuis [4] and repeated dispersals from Amazonian lineages since the Pliocene. However, the diversity of poison frogs in the Guiana Shield is only beginning to be revealed [48]. In contrast, diversification in the Venezuelan region most likely reflects the oldest vicariant event in Dendrobatidae, at 40.9 MYA. The costal ranges of Mérida, Cordillera de la Costa, and Paria peninsula are species rich but their total area is less than 5% of that of the Amazon Basin. No lineage of this endemic fauna has dispersed out to other regions since the early radiation of the poison frog family in the late Eocene. However, Eocene floristic paleoecological reconstruction of the Venezuelan Highlands area showed that it was more diverse than at present [49], suggesting that the ancestral habitat of the first poison frogs might have been lowland. The depauperate dendrobatid fauna of the Venezuelan llanos and Brazilian Shield plateau is puzzling, but might be related to Holocene aridity [50]. The recurring dispersals to Amazonia suggests that a large part of dendrobatid diversity results from repeated immigration waves at 75% of all possible reconstructions was used as the best solution and mapped on the ML poison frog phylogeny (Figure S7). For the third method, estimates of the values of states at ancestral nodes were derived by point estimates (log-likelihoods) using an ML approach in BAYESMULTISTATE, a component of BAYESTRAITS [79,100]. The reduced chronogram (236 terminals) described in the Materials and Methods section “Determination of divergence times” was used for the analysis. We coded all terminal distributions under two alternatives, Amazonian Basin (C) origin, and non-Amazonian Basin origin (all other areas). We calculated the proportion of likelihood of both alternatives at each node with 10,000 samples under default parameters. The results were mapped onto the chronogram (Figure 2). We also tested whether an Amazonian origin was present at each node by constraining the node to this state using the option “fossilizing” in BAYESMULTISTATE [100]. The likelihoods of the constrained and unconstrained reconstructions were compared, and a difference of ≥2 log-likelihood units was considered significant; the model with the worse score was rejected [99]. Speciation and extinction patterns under incomplete taxon sampling. We calculated the tree imbalance of the ML poison frog phylogeny, the reduced-taxon chronogram, and the tree of each super-regions: the Amazon Basin (region C), the Andes (regions E–H), Chocó-Central America (regions I and J), and Guiana Shield-Venezuela-Brazilian Shield (regions B, D, and K). We used conservative imbalance metrics [25,101]: IC [102], IS [103], and s [104,105]. All standardized indices and probability of rejecting the null model of each branch having the equal probability of splitting (Equal Markov Rate or ERM) were calculated using functions colless.test, sackin.test, and likelihood.test, implemented in the R package apTreeshape [106]. An indirect estimate of diversification rates assuming incomplete taxon sampling was explored using the γ statistic [32] and adjusted for actual phylogenies by excluding the distance between the most recent node to the present (i.e., g n node of a phylogeny of size n), which does not come from the same distribution [33]. The adjusted γ statistic value was obtained from the Poison Frog Chronogram (family level). The adjusted γ statistic [32,33] was calculated using following functions of the R package LASER [107]: (1) the gn node was excluded from the chronogram (i.e., entire family and major region subtrees) by using truncateTree function; (2) the γ statistic of the truncated tree was calculated using gamStat function; (3) a null-distribution of γ under a pure birth model was obtained by 10,000 Monte Carlo replicates using mccrTest.Rd. This function generates full size trees at the species level and prunes randomly terminals to the actual size of the empirical tree (i.e., simulates incomplete taxon sampling); (4) the empirical γ statistic was adjusted by subtracting the mean value of the simulated null-distribution of γ, which is expected to be 0 [33]; and (5) the p-values of the adjusted γ statistics were computed from a normal distribution; values outside the ±1.96 standard deviation boundaries are significantly different (alpha = 0.05) from the null pure birth expectation. We tested for significant changes in diversification rate within the poison frog clade using a ML methodology under the assumption of incomplete taxon sampling [36]. First, we produced a GSPF level chronogram by pruning all but a single lineage per taxonomic group (Figures 3 and S8; Table S13) from the Poison Frog Chronogram, yielding a tree of 78 terminals. The total species richness per taxonomic group was assigned to each terminal based on previous taxonomic and phylogenetic studies [22,23,108–112]. Second, we estimated a constant diversification rate r (i.e., the difference between speciation λ and extinction μ rates) across the phylogeny using a ML estimator that incorporates both known taxonomic diversity and phylogenetic data [36]. We calculated the constant-rate model fit statistics (log likelihood and AIC score) and r using the fitNDR_1rate.Rd function of LASER [107]. Third, we tested for shifts in diversification rate within the poison frog phylogeny by comparing likelihood of the GSPF chronogram under constant and rate-flexible diversification models [36]. Two alternative hypotheses for rate-flexible model may explain the shifts in rate of diversification: (1) an increase within a particular clade (r CL) from the ancestral diversification rate r (flexible-rate model) or (2) a clade-specific decrease (r CL) from the ancestral diversification rate r (rate-decrease model) [36]. We calculated both rate-flexible alternative model fit statistics, r and r CL values using the fitNDR_2rate.Rd function of LASER [107]. The best fitting model was determined using a likelihood ratio test (LRT) between the constant-rate and the flexible-rate models (nested), and by ΔAIC scores between the flexible-rate and rate-decrease models (not nested). All analyses were performed under two extremes of the relative extinction rate (α = μ/λ, α = 0 and α = 0.99) as a fixed parameter to determine the robustness of the results to variation in the extinction fraction [113]. Sequence accession numbers. GenBank (http://www.ncbi.nlm.nih.gov/Genbank) sequence accession numbers mentioned in this paper are EU342502–EU342745 (see Tables S2 and S3). Supporting Information Figure S1 Molecular Phylogeny of Amphibians Including 80 Species of Anurans (30 Families), Three Species of Salamanders (Three Families), Three Species of Caecilians (Three Families), and Three Outgroups (Lungfish, Human, and Chicken) The phylogram was produced under a genetic algorithm in GARLI 0.951 [64]. We also inferred the tree topology and branch lengths using a Bayesian sampling of tree space with MrBayes 3.1.2 [65,66]. Support values from the nodes were constructed with 200 nonparametric bootstrap replicates (above branch) and Bayesian posterior probabilities (below branch). An asterisk indicates a support value of 100. (5.20 MB JPG) Click here for additional data file. Figure S2 Molecular Chronogram of the Amphibians (80 Anuran, Three Salamander, and Three Caecilian Species) Used to Date the Origin and Divergence of Poison Frogs (Dendrobatidae) (a) Relaxed clock chronogram estimated from the ML tree using time constraints (date from seven fossils and one paleogeographic date constraints as in Table S4); support values for the nodes were constructed with 200 bootstrap replicates (ML) using GARLI; Bayesian posterior probabilities (PP) were estimated using MrBayes; gray bars are 95% CI of the estimated node age. Six major geological events are indicated by red squares: (1) rifting of Pangaea; (2) Gondwana break-up; (3) separation of South America from Africa; (4) Cretaceous–Tertiary mass extinction; (5) initial orogeny of the Andes; (6) formation of the modern Amazon Basin; (7) Stem Dendrobatidae; and (8) Dendrobatidae. (4.53 MB JPG) Click here for additional data file. Figure S3 Molecular Phylogeny of the Poison Frogs Inferred from 394 Individuals of 137 Described and 34–89 Undescribed Species (A–D) The phylogram is the ML methods under a genetic algorithm in GARLI 0.951 [64]. We also inferred the tree topology and branch lengths using a Bayesian sampling of tree space with MrBayes 3.1.2 [65,66]. Support values from the nodes were constructed with 200 nonparametric bootstrap replicates (above branch) and Bayesian posterior probabilities (below branch). (*) indicates that the support value was 100. The coding of the individual terminals includes the generic, species, locality, country code, biogeographic area, and museum, field series, or GenBank accession numbers (see Table S3). (2.55 MB PDF) Click here for additional data file. Figure S4 Node Numbers and Constraints of the Amphibian Chronogram Used in the Molecular Dating Analyses See Table S4. (4.38 MB JPG) Click here for additional data file. Figure S5 Node Numbers and Constraints of the Poison Frog Phylogeny Used in the Molecular Dating Analyses (A–D) The nodes preceded by “N” correspond to the ML phylogeny and those that were preceded by “#” correspond to the chronogram. See Table S5. (2.36 MB PDF) Click here for additional data file. Figure S6 Geographic Scenarios for Diversification of Poison Frogs (1) SM0, the null model, assumes no spatial structure, with equal rates of dispersal among all areas and no constraints on ancestral range composition; (2) alternative center of origin model SM1 models the dispersal rate into and out of the Amazonia as twice the rate between all other areas, with widespread ancestral ranges constrained to include the Amazon Basin; and (3) a stepping-stone model SM2 accounts for area adjacency, scaling rates of dispersal between areas inversely by relative distance, and constraining widespread ancestors to spatially adjacent areas. Each hypothesis test was repeated in the large ML phylogeny and in the chronogram. The area codes correspond to Guiana Shield (B), Amazon Basin (C), Venezuela Highlands and Trinidad and Tobago Islands (D), Northern Andean Cordillera Oriental (E), Northern Andean Cordillera Occidental (F), Central Andean Cordillera Oriental (G), Central Andean Cordillera Occidental (H), Chocó, Magdalena Valley, and Gorgona Island (I), Central America (J), and Brazilian Shield (K). (814 KB JPG) Click here for additional data file. Figure S7 The Ancestral Areas Inferred from DIVA and DEC Model using Lagrange, Mapped Over the Complete ML Tree Reconstruction The “?” corresponds to Allobates alagoanus, whose phylogenetic relationships are uncertain [26,30,77]. (7.57 MB JPG) Click here for additional data file. Figure S8 The GSPF Level Chronogram with the Species Groups Used for the Diversification Analyses Node numbers correspond to those provided in Figure S5A–S5D that match the ML phylogeny. (5.04 MB JPG) Click here for additional data file. Table S1 Tree Imbalance Indices (Colless IC , Sackin IS , and Likelihood Shape s) Estimated for the Poison Frog Chronogram, the Trees for Each Super-Region and the Corresponding Probability of Rejecting the Null Equal Markov Rate An asterisk indicates significance at α = 0.05. (49 KB PDF) Click here for additional data file. Table S2 Taxa Used to Infer the Age of the Root of the Poison Frog Tree Including GenBank Accession Numbers of Genes Used (82 KB PDF) Click here for additional data file. Table S3 Taxa Used to Infer the Phylogeny and the Chronogram of the Poison Frogs “Use” identifies which samples were used for the phylogeny (P), chronogram (C), and Langrage (L) analyses. Other columns provide GenBank accession numbers, locality of collection, and biogeographic region of the Neotropics. (305 KB PDF) Click here for additional data file. Table S4 Time Constraints Used to Infer the Age of the Root of the Poison Frog Tree (94 KB PDF) Click here for additional data file. Table S5 Poison Frog Time Constraints Node numbers are indicated in the Figure S5A–S5D. (107 KB PDF) Click here for additional data file. Table S6 Published Evidence Supporting the Paleogeographic Constraints Used in Inferring the Poison Frog Chronogram (111 KB PDF) Click here for additional data file. Table S7 Amphibian Tree estimated Divergence Times for MULTIDIVTIME Nodes from Figure S4A–S4D. (74 KB PDF) Click here for additional data file. Table S8 Poison Frog Tree Estimated Divergence Times, Events (Vicariance and Dispersals), Lagrange Ancestral Area Reconstructions, and BayesTraits Probability of Amazon Basin Area at the Chronogram Node Node numbers form Figure S5A–S5D. (124 KB PDF) Click here for additional data file. Table S9 Poison Frog Tree Estimated Divergence Times of Taxonomic Events and Results of the Chronogram Calibration Robustness and Constraint Reliability Analysis (A) corresponds to the node age estimations using MULTIDIVTIME constraint jackknifing and “bigtime” prior variation. (B) corresponds to the node age estimations using penalized likelihood approach (r8s) [71] constraint jackknifing. Node numbers form Figure S5A–S5D. (142 KB PDF) Click here for additional data file. Table S10 Node Time Differences between the Chronogram Age Mean and Those of the Jackknifed Constraint Estimated Chronograms for Both r8s and MULTIDIVTIME Bold indicate difference (V), that is 2 SD > V > 1 SD of the TimeSet 1 chronogram. Node numbers form Figure S5A–S5D. (72 KB PDF) Click here for additional data file. Table S11 Species of Poison Frogs Not Included in the Analyses with Information about the Author of the Species Description, Distribution, Range, Area of Distribution, Phylogenetic Group, and Conservation Status from Global Amphibian Assessment (GAA) (196 KB PDF) Click here for additional data file. Table S12 Poison Frog Tree Dispersal Events Indicated in Figure 2 with Their Estimated Divergence Times and Node Number from the ML Phylogeny Node numbers form Figure S5A–S5D. (65 KB PDF) Click here for additional data file. Table S13 Poison Frog Species Group and Taxonomic Diversity Assigned to the Diversification Rate Analyses and Figure 3 The species sampled for the analyses are indicated by “*”. (62 KB PDF) Click here for additional data file. Table S14 Diversification Rate Estimates under the Flexible-Rate Model with the Lowest Extinction Fraction (a = 0 and a = 0.99) Node numbers correspond to Figure S8. (94 KB PDF) Click here for additional data file. Text S1 Corrections to the Poison Frog Taxonomy and Supporting Literature for Tables S4–S6 (52 KB DOC) Click here for additional data file.
Author and article information
Contributors
Eva Ringler:
ORCID: http://orcid.org/0000-0003-3273-6568
eva.ringler@vetmeduni.ac.at
Journal
Journal ID (nlm-ta): Mol Ecol
Journal ID (iso-abbrev): Mol. Ecol
Journal ID (doi): 10.1111/(ISSN)1365-294X
Journal ID (publisher-id): MEC
Title:
Molecular Ecology
Publisher:
John Wiley and Sons Inc.
(Hoboken
)
ISSN
(Print):
0962-1083
ISSN
(Electronic):
1365-294X
Publication date
(Electronic):
23
April
2018
Publication date
(Print):
May
2018
Volume: 27
Issue: 9
(
doiID:
10.1111/mec.2018.27.issue-9
)
Pages: 2289-2301
Affiliations
[
1
]
Department of Integrative Biology and Physiology
University of California Los Angeles
Los Angeles
California
[
2
]
Messerli Research Institute
University of Veterinary Medicine Vienna, Medical University of Vienna, University
of Vienna
Vienna
Austria
Author notes
[*]
[*
]
Correspondence
Eva Ringler, Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA.
Email: eva.ringler@ 123456vetmeduni.ac.at
Eva Ringler, Department of Integrative Biology and Physiology, University of California Los Angeles, Los Angeles, CA.
Email: eva.ringler@ 123456vetmeduni.ac.at
Author information
Eva Ringler
http://orcid.org/0000-0003-3273-6568
Article
Publisher ID: MEC14583DOI: 10.1111/mec.14583
PMC ID: 5969290
PubMed ID: 29633409
SO-VID: cc80df3f-a32b-4ce6-a158-c9dd0a3accb5
Copyright © © 2018 The Authors.
Molecular Ecology Published by John Wiley & Sons Ltd
License:
This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
History
Date
received
: 01
December
2017
Date
revision received
: 28
January
2018
Date
accepted
: 23
February
2018
Page count
Figures: 5,
Tables: 0,
Pages: 13,
Words: 10413
Funding
Funded by: Austrian Science Fund
Award ID: P24788‐B22
Funded by: Hertha Firnberg Fellowship
Award ID: T699‐B24
Funded by: Erwin‐Schrödinger Fellowship
Award ID: J3868‐B29
Funded by: Agence Nationale de la Recherche
Award ID: ANR‐11‐INBS‐0001
Funded by: Labex CEBA
Award ID: ANR‐10‐LABX‐25‐01
Categories
Subject:
Original Article
Subject:
ORIGINAL ARTICLES
Subject:
Kinship, Parentage and Behaviour
Custom metadata
source-schema-version-number 2.0
component-id mec14583
cover-date May 2018
details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_NLMPMC version:version=5.3.8.2 mode:remove_FC converted:25.05.2018
ScienceOpen disciplines: Ecology
Data availability:
ScienceOpen disciplines: Ecology