Diversification of unicellular eukaryotes: cryptomonad colonizations of marine and fresh waters inferred from revised 18S rRNA phylogeny

The cryptomonads is a well-defined lineage of unicellular eukaryotes, composed of several marine and freshwater groups. However, the evolutionary relationships among these groups are unclear due to conflicting inferences between morphological and molecular phylogenies. Here, we have inferred the evolutionary relationships among marine and freshwater species in order to better understand the importance of the marine-freshwater boundary on the historical diversification patterns of cryptomonads. We have constructed improved molecular phylogenies by taking into account rate variation both across sites and across sequences (covarion substitutions), and by analysing the vast majority of publicly available cryptomonad 18S rRNA sequences and related environmental phylotypes. The resulting phylogenies included 55 sequences, and revealed two novel freshwater cryptomonad clades (CRY1 and CRY2) and a large hidden diversity of cryptomonads. CRY1 was placed deeply within the cryptomonad phylogeny together with all the major freshwater lineages (i.e. Goniomonas and Cryptomonas), while CRY2 was placed within a lineage of marine species identified as Plagioselmis-like with the aid of a new sequence generated from a cultured species. The inferred phylogenies suggest only few successful marine-freshwater transitions over the history of cryptomonads. Most of the transitions seem to have occurred from marine to fresh waters, but re-colonizations of marine habitats have also taken place. This implies that the differences in the biogeophysical conditions between marine and fresh waters constitute a substantial barrier for the cross-colonization of these environments by cryptomonads.     

Cenozoic climate change and diversification on the continental shelf and slope: evolution of gastropod diversity in the family Solariellidae (Trochoidea)

Recent expeditions have revealed high levels of biodiversity in the tropical deep‐sea, yet little is known about the age or origin of this biodiversity, and large‐scale molecular studies are still few in number. In this study, we had access to the largest number of solariellid gastropods ever collected for molecular studies, including many rare and unusual taxa. We used a Bayesian chronogram of these deep‐sea gastropods (1) to test the hypothesis that deep‐water communities arose onshore, (2) to determine whether Antarctica acted as a source of diversity for deep‐water communities elsewhere and (3) to determine how factors like global climate change have affected evolution on the continental slope. We show that although fossil data suggest that solariellid gastropods likely arose in a shallow, tropical environment, interpretation of the molecular data is equivocal with respect to the origin of the group. On the other hand, the molecular data clearly show that Antarctic species sampled represent a recent invasion, rather than a relictual ancestral lineage. We also show that an abrupt period of global warming during the Palaeocene Eocene Thermal Maximum (PETM) leaves no molecular record of change in diversification rate in solariellids and that the group radiated before the PETM. Conversely, there is a substantial, although not significant increase in the rate of diversification of a major clade approximately 33.7 Mya, coinciding with a period of global cooling at the Eocene–Oligocene transition. Increased nutrients made available by contemporaneous changes to erosion, ocean circulation, tectonic events and upwelling may explain increased diversification, suggesting that food availability may have been a factor limiting exploitation of deep‐sea habitats. Tectonic events that shaped diversification in reef‐associated taxa and deep‐water squat lobsters in central Indo‐West Pacific were also probably important in the evolution of solariellids during the Oligo‐Miocene.     

Insights in the ecology and evolutionary history of the Miscellaneous Crenarchaeotic Group lineage

Members of the archaeal Miscellaneous Crenarchaeotic Group (MCG) are among the most successful microorganisms on the planet. During its evolutionary diversification, this very diverse group has managed to cross the saline–freshwater boundary, one of the most important evolutionary barriers structuring microbial communities. However, the current understanding on the ecological significance of MCG in freshwater habitats is scarce and the evolutionary relationships between freshwater and saline MCG remains poorly known. Here, we carried out molecular phylogenies using publicly available 16S rRNA gene sequences from various geographic locations to investigate the distribution of MCG in freshwater and saline sediments and to evaluate the implications of saline–freshwater transitions during the diversification events. Our approach provided a robust ecological framework in which MCG archaea appeared as a core generalist group in the sediment realm. However, the analysis of the complex intragroup phylogeny of the 21 subgroups currently forming the MCG lineage revealed that distinct evolutionary MCG subgroups have arisen in marine and freshwater sediments suggesting the occurrence of adaptive evolution specific to each habitat. The ancestral state reconstruction analysis indicated that this segregation was mainly due to the occurrence of a few saline–freshwater transition events during the MCG diversification. In addition, a network analysis showed that both saline and freshwater MCG recurrently co-occur with archaea of the class Thermoplasmata in sediment ecosystems, suggesting a potentially relevant trophic connection between the two clades.     

Deep-sea squat lobster biogeography (Munidopsidae: Leiogalathea) unveils Tethyan vicariance and evolutionary patterns shared by shallow-water relatives

The ecology, abundance and diversity of galatheoid squat lobsters make them an ideal group to study deep-sea diversification processes. Here, we reconstructed the evolutionary and biogeographic history of Leiogalathea, a genus of circum-tropical deep-sea squat lobsters, in order to compare patterns and processes that have affected shallow-water and deep-sea squat lobster species. We first built a multilocus phylogeny and a calibrated species tree with a relaxed clock using StarBEAST2 to reconstruct evolutionary relationships and divergence times among Leiogalathea species. We used BioGeoBEARS and a DEC model, implemented in RevBayes, to reconstruct ancestral distribution ranges and the biogeographic history of the genus. Our results showed that Leiogalathea is monophyletic and comprises four main lineages; morphological homogeneity is common within and between clades, except in one; the reconstructed ancestral range of the genus is in the Atlantic and Indian oceans (Tethys). They also revealed the divergence of the Atlantic species around 25 million years ago (Ma), intense cladogenesis 15–25 Ma and low levels of speciation over the last 5 million years (Myr). The four Leiogalathea lineages showed similar patterns of speciation: allopatric speciation followed by range expansion and subsequent stasis. Leiogalathea started diversifying during the Oligocene, likely in the Tethyan. The Atlantic lineage then split from its Indo-Pacific sister group due to vicariance driven by closure of the Tethys Seaway. The Atlantic lineage is less speciose compared with the Indo-Pacific lineages, with the Tropical Southwestern Pacific being the current centre of diversity. Leiogalathea diversification coincided with cladogenetic peaks in shallow-water genera, indicating that historical biogeographic events similarly shaped the diversification and distribution of both deep-sea and shallow-water squat lobsters.     

Molecular signatures of Pleistocene sea-level changes that affected connectivity among freshwater shrimp in Indo-Australian waters

A major paradigm in evolutionary biology asserts that global climate change during the Pleistocene often led to rapid and extensive diversification in numerous taxa. Recent phylogenetic data suggest that past climatic oscillations may have promoted long-distance marine dispersal in some freshwater crustacea from the Indo-Australian Archipelago (IAA). Whether this pattern is common, and whether similar processes are acting on diversification below the species level is unknown. We used nuclear and mitochondrial molecular variation in a freshwater-dependent decapod crustacean (Macrobrachium rosenbergii), sampled widely from the IAA, to assess the impact of Pleistocene sea-level changes on lineage diversification in this species. Fitting of an isolation with migration model enabled us to reject ongoing migration among lineages, and results indicate that isolation among both mainland-mainland and mainland-island lineages arose during the mid-Pleistocene. Our data suggest a scenario of widespread marine dispersal during Pleistocene glacial maxima (in support of the 'Pleistocene marine dispersal hypothesis') when sea levels were low, and geographical distances between fresh watersheds were greatly reduced, followed by increased isolation as sea levels subsequently rose.     

Molecular phylogeny of extant horseshoe crabs (Xiphosura, Limulidae) indicates Paleogene diversification of Asian species

Horseshoe crabs are marine invertebrates well known for their exceptionally low rates of diversification during their entire evolutionary history. Despite the low species diversity in the group, the phylogenetic relationships among the extant species, especially among the three Asian species are still unresolved. Here we apply a new set of molecular genetic data in combination with a wide geographic sampling of the intra-specific diversity to reinvestigate the evolutionary history among the four living limulid xiphosurans. Our analysis of the intraspecific diversity reveals low levels of connectivity among Carcinoscorpius rotundicauda lineages, which can be explained by the estuarine-bound ecology of this species. Moreover, a clear genetic break across the Thai-Malay Peninsula suggests the presence of cryptic species in C. rotundicauda. The limulid phylogeny finds strong support for a monophyletic genus Tachypleus and a diversification of the three Asian species during the Paleogene period, with speciation events well separated in time by several million years. The tree topology suggests that the three Asian species originated in central South East Asia from a marine stem group that inhabited the shallow coastal waters between the Andaman Sea, Vietnam, and Borneo. In this region C. rotundicauda probably separated from the Tachypleus stem group by invading estuarine habitats, while Tachypleus tridentatus most likely migrated northeast along the Southern coast of China and towards Japan.     

Phylogenetic characterization of three morphs of mussels (Bivalvia, Mytilidae) inhabiting isolated marine environments in Palau Islands

Marine lakes in the Palau Islands are known to harbor unique marine fauna that have remained isolated since the formation of the lakes after the Last Glacial Maximum. We analyzed mussels from marine lakes located on different islands and conducted morphological, phylogenetic and population genetic characterization to clarify their evolutionary history. The mussels were morphologically classified into three differentiated morphs: NS, ON, and MC. Their common characteristics were consistent with the Brachidontes-Hormomya complex of the Mytilidae family. Phylogenetic analysis based on the nuclear 18S ribosomal RNA gene supported the taxonomic position of the mussels among the Mytilidae. In the mitochondrial cytochrome c oxidase subunit I (COI) gene lineage, NS-and MC-morphs were highly diverged from each other; their estimated time of divergence dates back to the mid-Pleistocene. ON-morph was more closely related to MC-morph, although the shell morphologies of ON- and MC-morphs were easily distinguishable. Population genetic analysis revealed the coexistence of highly diverged haplotypes within a population of ON-morph, indicating introgression of mtDNA among the morphs. Our data suggest that morphological differentiation of marine lake mussels can occur in a relatively short period under different environmental conditions. Thus, the marine lakes provide a unique site for the study of diversification in mussels.     

Rapid speciation and ecological divergence in the American seven-spined gobies (Gobiidae,Gobiosomatini) inferred from a molecular phylogeny

Abstract.— The American seven-spined gobies (Gobiidae, Gobiosomatini) are highly diverse both in morphology and ecology with many endemics in the Caribbean region. We have reconstructed a molecular phylogeny of 54 Gobio-somatini taxa (65 individuals) based on a 1646-bp region that includes the mitochondrial 12S rRNA, tRNA-Val, and 16S rRNA genes. Our results support the monophyly of the seven-spined gobies and are in agreement with the existence of two major groups within the tribe, the Gobiosoma group and the Microgobius group. However, they reject the monophyly of some of the Gobiosomatini genera. We use the molecular phylogeny to study the dynamics of speciation in the Gobiosomatini by testing for departures from the constant speciation rate model. We observe a burst of speciation in the early evolutionary history of the group and a subsequent slowdown. Our results show a split among clades into coastal-estuarian, deep ocean, and tropical reef habitats. Major habitat shifts account for the early significant acceleration in lineage splitting and speciation rate and the initial divergence of the main Gobiosomatini clades. We found that subsequent diversification is triggered by behavior and niche specializations at least in the reef-associated clades. Overall, our results confirm that the diversity of Gobiosomatini has arisen during episodes of adaptive radiation, and emphasize the importance of ecology in marine speciation.     

BOOM AND BUST: ANCIENT AND RECENT DIVERSIFICATION IN BICHIRS (POLYPTERIDAE: ACTINOPTERYGII), A RELICTUAL LINEAGE OF RAY‐FINNED FISHES

Understanding the history that underlies patterns of species richness across the Tree of Life requires an investigation of the mechanisms that not only generate young species‐rich clades, but also those that maintain species‐poor lineages over long stretches of evolutionary time. However, diversification dynamics that underlie ancient species‐poor lineages are often hidden due to a lack of fossil evidence. Using information from the fossil record and time calibrated molecular phylogenies, we investigate the history of lineage diversification in Polypteridae, which is the sister lineage of all other ray‐finned fishes (Actinopterygii). Despite originating at least 390 million years (Myr) ago, molecular timetrees support a Neogene origin for the living polypterid species. Our analyses demonstrate polypterids are exceptionally species depauperate with a stem lineage duration that exceeds 380 million years (Ma) and is significantly longer than the stem lineage durations observed in other ray‐finned fish lineages. Analyses of the fossil record show an early Late Cretaceous (100.5–83.6 Ma) peak in polypterid genus richness, followed by 60 Ma of low richness. The Neogene species radiation and evidence for high‐diversity intervals in the geological past suggest a “boom and bust” pattern of diversification that contrasts with common perceptions of relative evolutionary stasis in so‐called “living fossils.”     

Density-dependent diversification in North American wood warblers

Evidence from both molecular phylogenies and the fossil record suggests that rates of species diversification often decline through time during evolutionary radiations. One proposed explanation for this pattern is ecological opportunity, whereby an initial abundance of resources and lack of potential competitors facilitate rapid diversification. This model predicts density-dependent declines in diversification rates, but has not been formally tested in any species-level radiation. Here we develop a new conceptual framework that distinguishes density dependence from alternative processes that also produce temporally declining diversification, and we demonstrate this approach using a new phylogeny of North American Dendroica wood warblers. We show that explosive lineage accumulation early in the history of this avian radiation is best explained by a density-dependent diversification process. Our results suggest that the tempo of wood warbler diversification was mediated by ecological interactions among species and that lineage and ecological diversification in this group are coupled, as predicted under the ecological opportunity model.     

Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago

Speciation remains a central enigma in biology, and nowhere is this more apparent than in shallow tropical seas where biodiversity rivals that of tropical rainforests. Obvious barriers to gene flow are few and most marine species have a highly dispersive larval stage, which should greatly decrease opportunities for speciation via geographic isolation. The disparity in the level of geographic isolation for terrestrial and marine species is exemplified in Hawai'i where opportunities for allopatric speciation abound in the terrestrial realm. In contrast, marine colonizers of Hawai'i are believed to produce only a single endemic species or population, due to the lack of isolating barriers. To test the assertion that marine species do not diversify within Hawai'i, we examine the evolutionary origin of three endemic limpets (Cellana exarata, C. sandwicensis and C. talcosa) that are vertically segregated across a steep ecocline on rocky shores. Analyses of three mtDNA loci (12S, 16S, COI; 1565bp) and two nDNA loci (ATPSβ, H3; 709bp) in 26 Indo-Pacific Cellana species (N=414) indicates that Hawai'i was colonized once ～3.4-7.2Ma from the vicinity of Japan. Trait mapping demonstrates that high-shore residence is the ancestral character state, such that mid- and low-shore species are the product of subsequent diversification. The Hawaiian Cellana are the first broadcast-spawners demonstrated to have speciated within any archipelago. The habitat stratification, extensive sympatry, and evolutionary history of these limpets collectively indicate a strong ecological component to speciation and support the growing body of evidence for non-allopatric speciation in the ocean.     

Comparative Analysis of Japanese Three-Spined Stickleback Clades Reveals the Pacific Ocean Lineage Has Adapted to Freshwater Environments while the Japan Sea Has Not

Divergent selection and adaptive divergence can increase phenotypic diversification amongst populations and lineages. Yet adaptive divergence between different environments, habitats or niches does not occur in all lineages. For example, the colonization of freshwater environments by ancestral marine species has triggered adaptive radiation and phenotypic diversification in some taxa but not in others. Studying closely related lineages differing in their ability to diversify is an excellent means of understanding the factors promoting and constraining adaptive evolution. A well-known example of the evolution of increased phenotypic diversification following freshwater colonization is the three-spined stickleback. Two closely related stickleback lineages, the Pacific Ocean and the Japan Sea occur in Japan. However, Japanese freshwater stickleback populations are derived from the Pacific Ocean lineage only, suggesting the Japan Sea lineage is unable to colonize freshwater. Using stable isotope data and trophic morphology, we first show higher rates of phenotypic and ecological diversification between marine and freshwater populations within the Pacific Ocean lineage, confirming adaptive divergence has occurred between the two lineages and within the Pacific Ocean lineage but not in the Japan Sea lineage. We further identified consistent divergence in diet and foraging behaviour between marine forms from each lineage, confirming Pacific Ocean marine sticklebacks, from which all Japanese freshwater populations are derived, are better adapted to freshwater environments than Japan Sea sticklebacks. We suggest adaptive divergence between ancestral marine populations may have played a role in constraining phenotypic diversification and adaptive evolution in Japanese sticklebacks.     

Lineage diversification and morphological evolution in a large-scale continental radiation: the neotropical ovenbirds and woodcreepers (aves: Furnariidae)

Patterns of diversification in species-rich clades provide insight into the processes that generate biological diversity. We tested different models of lineage and phenotypic diversification in an exceptional continental radiation, the ovenbird family Furnariidae, using the most complete species-level phylogenetic hypothesis produced to date for a major avian clade (97% of 293 species). We found that the Furnariidae exhibit nearly constant rates of lineage accumulation but show evidence of constrained morphological evolution. This pattern of sustained high rates of speciation despite limitations on phenotypic evolution contrasts with the results of most previous studies of evolutionary radiations, which have found a pattern of decelerating diversity-dependent lineage accumulation coupled with decelerating or constrained phenotypic evolution. Our results suggest that lineage accumulation in tropical continental radiations may not be as limited by ecological opportunities as in temperate or island radiations. More studies examining patterns of both lineage and phenotypic diversification are needed to understand the often complex tempo and mode of evolutionary radiations on continents.     

Reconciling extreme branch length differences: decoupling time and rate through the evolutionary history of filmy ferns

The rate of molecular evolution is not constant across the Tree of Life. Characterizing rate discrepancies and evaluating the relative roles of time and rate along branches through the past are both critical to a full understanding of evolutionary history. In this study, we explore the interactions of time and rate in filmy ferns (Hymenophyllaceae), a lineage with extreme branch length differences between the two major clades. We test for the presence of significant rate discrepancies within and between these clades, and we separate time and rate across the filmy fern phylogeny to simultaneously yield an evolutionary time scale of filmy fern diversification and reconstructions of ancestral rates of molecular evolution. Our results indicate that the branch length disparity observed between the major lineages of filmy ferns is indeed due to a significant difference in molecular evolutionary rate. The estimation of divergence times reveals that the timing of crown group diversification was not concurrent for the two lineages, and the reconstruction of ancestral rates of molecular evolution points to a substantial rate deceleration in one of the clades. Further analysis suggests that this may be due to a genome-wide deceleration in the rate of nucleotide substitution.     

Out of the blue: adaptive visual pigment evolution accompanies Amazon invasion

Incursions of marine water into South America during the Miocene prompted colonization of freshwater habitats by ancestrally marine species and present a unique opportunity to study the molecular evolution of adaptations to varying environments. Freshwater and marine environments are distinct in both spectra and average intensities of available light. Here, we investigate the molecular evolution of rhodopsin, the photosensitive pigment in the eye that activates in response to light, in a clade of South American freshwater anchovies derived from a marine ancestral lineage. Using likelihood-based comparative sequence analyses, we found evidence for positive selection in the rhodopsin of freshwater anchovy lineages at sites known to be important for aspects of rhodopsin function such as spectral tuning. No evidence was found for positive selection in marine lineages, nor in three other genes not involved in vision. Our results suggest that an increased rate of rhodopsin evolution was driven by diversification into freshwater habitats, thereby constituting a rare example of molecular evolution mirroring large-scale palaeogeographic events.     

DO FRESHWATER FISHES DIVERSIFY FASTER THAN MARINE FISHES? A TEST USING STATE‐DEPENDENT DIVERSIFICATION ANALYSES AND MOLECULAR PHYLOGENETICS OF NEW WORLD SILVERSIDES (ATHERINOPSIDAE)

Freshwater habitats make up only ～0.01% of available aquatic habitat and yet harbor 40% of all fish species, whereas marine habitats comprise >99% of available aquatic habitat and have only 60% of fish species. One possible explanation for this pattern is that diversification rates are higher in freshwater habitats than in marine habitats. We investigated diversification in marine and freshwater lineages in the New World silverside fish clade Menidiinae (Teleostei, Atherinopsidae). Using a time‐calibrated phylogeny and a state‐dependent speciation–extinction framework, we determined the frequency and timing of habitat transitions in Menidiinae and tested for differences in diversification parameters between marine and freshwater lineages. We found that Menidiinae is an ancestrally marine lineage that independently colonized freshwater habitats four times followed by three reversals to the marine environment. Our state‐dependent diversification analyses showed that freshwater lineages have higher speciation and extinction rates than marine lineages. Net diversification rates were higher (but not significant) in freshwater than marine environments. The marine lineage‐through time (LTT) plot shows constant accumulation, suggesting that ecological limits to clade growth have not slowed diversification in marine lineages. Freshwater lineages exhibited an upturn near the recent in their LTT plot, which is consistent with our estimates of high background extinction rates. All sequence data are currently being archived on Genbank and phylogenetic trees archived on Treebase.     

High tropical net diversification drives the New World latitudinal gradient in palm (Arecaceae) species richness

Aim Species richness exhibits striking geographical variation, but the processes that drive this variation are unresolved. We investigated the relative importance of two hypothesized evolutionary causes for the variation in palm species richness across the New World: time for diversification and evolutionary (net diversification) rate. Palms have a long history in the region, with the major clades diversifying during the Tertiary (65–2 Ma). Location Tropical and subtropical America (34° N–34° S; 33–120° W). Methods Using range maps, palm species richness was estimated in a 1° × 1° grid. Mean lineage net diversification was estimated by the mean phylogenetic root distance (MRD), the average number of nodes separating a species from the base of the palm phylogeny for the species in each grid cell. If evolutionary rate limits richness, then richness should increase with MRD. If time limits richness, then old, relict species (with low root distance) should predominantly occur in long‐inhabited and therefore species‐rich areas. Hence, richness should decrease with MRD. To determine the influence of net diversification across different time frames, MRD was computed for subtribe, genus and species levels within the phylogeny, and supplemented with the purely tip‐level measure, mean number of species per genus (MS/G). Correlations and regressions, in combination with eigenvector‐based spatial filtering, were used to assess the relationship between species richness, the net diversification measures, and potential environmental and geographical drivers. Results Species richness increased with all net diversification measures. The regression models showed that richness and the net diversification measures increased with decreasing (absolute) latitude and, less strongly, with increasing energy/temperature and water availability. These patterns therefore reflect net diversification at both deep and shallow levels in the phylogeny. Richness also increased with range in elevation, but this was only reflected in the MS/G pattern and therefore reflects recent diversification. Main conclusions The geographical patterns in palm species richness appear to be predominantly the result of elevated net diversification rates towards the equator and in warm, wet climates, sustained throughout most of the Tertiary. Late‐Tertiary orogeny has caused localized increases in net diversification rates that have also made a mark on the richness pattern.     

Innovation not recovery: dynamic redox promotes metazoan radiations

Environmental fluctuations in redox may reinforce rather than hinder evolutionary transitions, such that variability in near‐surface oceanic oxygenation can promote morphological evolution and novelty. Modern, low‐oxygen regions are heterogeneous and dynamic habitats that support low diversity and are inhabited by opportunistic and non‐skeletal metazoans. We note that several major radiation episodes follow protracted or repeating intervals (>1 million years) of persistent and dynamic shallow marine redox (oceanic anoxic events). These are also often associated with short‐lived mass‐extinction events (<0.5 million years) where skeletal benthic incumbents are removed, and surviving or newly evolved benthos initially inhabit transient oxic habitats. We argue that such intervals create critical opportunities for the generation of evolutionary novelty, followed by innovation and diversification. We develop a general model for redox controls on the distribution and structure of the shallow marine benthos in a dominantly anoxic world, and compile data from the terminal Ediacaran–mid‐Cambrian (∼560–509 Ma), late Cambrian–Ordovician (∼500–445 Ma), and Permo‐Triassic (∼255–205 Ma) to test these predictions. Assembly of phylogenetic data shows that prolonged and widespread anoxic intervals indeed promoted morphological novelty in soft‐bodied benthos, providing the ancestral stock for subsequently skeletonized lineages to appear as innovations once oxic conditions became widespread and stable, in turn promoting major evolutionary diversification. As a result, we propose that so‐called ‘recovery’ intervals after mass extinctions might be better considered as ‘innovation’ intervals.     

Adaptive Evolution of Deep-Sea Amphipods from the Superfamily Lysiassanoidea in the North Atlantic

In this study we reconstruct phylogenies for deep sea amphipods from the North Atlantic in order to test hypotheses about the evolutionary mechanisms driving speciation in the deep sea. We sequenced five genes for specimens representing 21 families. Phylogenetic analyses showed incongruence between the molecular data and morphological taxonomy, with some morphologically distinct taxa showing close molecular similarity. Approximate dating of nodes based on available calibration suggested adaptation to the deep sea around the Cretaceous-Palaeogene boundary, with three identified lineages within the deep-sea radiation dating to the Eocene–Oligocene transition. Two of those lineages contained species currently classified in multiple families. We reconstructed ancestral nodes based on the mouthpart characters that define trophic guilds (also used to establish the current taxonomy), and show a consistent transition at the earliest node defining the deep-sea lineage, together with increasing diversification at more recent nodes within the deep-sea lineage. The data suggest that the divergence of species was adaptive, with successive diversification from a non-scavenging ancestor to ‘opportunistic’, ‘obligate’ and ‘specialised’ scavengers. We propose that the North Atlantic species studied provide a strong case for adaptive evolution promoted by ecological opportunity in the deep sea.     

Life-history specialization was not an evolutionary dead-end in Pyrenean cave beetles

Research on subterranean organisms has focused on the colonization process and some of the associated phenotypic changes, but little is known on the long-term evolutionary dynamics of subterranean lineages and the origin of some highly specialized complex characters. One of the most extreme modifications is the reduction of the number of larval instars in some Leptodirini beetles from the ancestral 3 to 2 and ultimately a single instar. This reduction is usually assumed to have occurred independently multiple times within the same lineage and geographical area, but its evolution has never been studied in a phylogenetic framework. Using a comprehensive molecular phylogeny, we found a low number of independent origins of the reduction in the number of instars, with a single transition, dated to the Oligocene–Miocene, from 3 to 2 and then 1 instar in the Pyrenees, the best-studied area. In the Pyrenees, the 1-instar lineage had a diversification rate (0.22 diversification events per lineage per million years) significantly higher than that of 3- or 2-instar lineages (0.10), and similar to that seen in other Coleopteran radiations. Far from being evolutionary dead-ends, ancient lineages fully adapted to subterranean life seem able to persist and diversify over long evolutionary periods.