Evolution of niche width and adaptive diversification

Theoretical models suggest that resource competition can lead to the adaptive splitting of consumer populations into diverging lineages, that is, to adaptive diversification. In general, diversification is likely if consumers use only a narrow range of resources and thus have a small niche width. Here we use analytical and numerical methods to study the consequences for diversification if the niche width itself evolves. We found that the evolutionary outcome depends on the inherent costs or benefits of widening the niche. If widening the niche did not have costs in terms of overall resource uptake, then the consumer evolved a niche that was wide enough for disruptive selection on the niche position to vanish; adaptive diversification was no longer observed. However, if widening the niche was costly, then the niche widths remained relatively narrow, allowing for adaptive diversification in niche position. Adaptive diversification and speciation resulting from competition for a broadly distributed resource is thus likely if the niche width is fixed and relatively narrow or free to evolve but subject to costs. These results refine the conditions for adaptive diversification due to competition and formulate them in a way that might be more amenable for experimental investigations.     

Symbiosis catalyses niche expansion and diversification

Interactions between species are important catalysts of the evolutionary processes that generate the remarkable diversity of life. Symbioses, conspicuous and inherently interesting forms of species interaction, are pervasive throughout the tree of life. However, nearly all studies of the impact of species interactions on diversification have concentrated on competition and predation leaving unclear the importance of symbiotic interaction. Here, I show that, as predicted by evolutionary theories of symbiosis and diversification, multiple origins of a key innovation, symbiosis between gall-inducing insects and fungi, catalysed both expansion in resource use (niche expansion) and diversification. Symbiotic lineages have undergone a more than sevenfold expansion in the range of host-plant taxa they use relative to lineages without such fungal symbionts, as defined by the genetic distance between host plants. Furthermore, symbiotic gall-inducing insects are more than 17 times as diverse as their non-symbiotic relatives. These results demonstrate that the evolution of symbiotic interaction leads to niche expansion, which in turn catalyses diversification.     

Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation

Antarctic notothenioid fishes represent a rare example of a marine species flock. They evolved special adaptations to the extreme environment of the Southern Ocean including antifreeze glycoproteins. Although lacking a swim bladder, notothenioids have diversified from their benthic ancestor into a wide array of water column niches, such as epibenthic, semipelagic, cryopelagic and pelagic habitats. Applying stable carbon (C) and nitrogen (N) isotope analyses to gain information on feeding ecology and foraging habitats, we tested whether ecological diversification along the benthic–pelagic axis followed a single directional trend in notothenioids, or whether it evolved independently in several lineages. Population samples of 25 different notothenioid species were collected around the Antarctic Peninsula, the South Orkneys and the South Sandwich Islands. The C and N stable isotope signatures span a broad range (mean δ¹³C and δ¹⁵N values between ?25.4‰ and ?21.9‰ and between 8.5‰ and 13.8‰, respectively), and pairwise niche overlap between four notothenioid families was highly significant. Analysis of isotopic disparity‐through‐time on the basis of Bayesian inference and maximum‐likelihood phylogenies, performed on a concatenated mitochondrial (cyt b) and nuclear gene (myh6, Ptr and tbr1) data set (3148 bp), showed that ecological diversification into overlapping feeding niches has occurred multiple times in parallel in different notothenioid families. This convergent diversification in habitat and trophic ecology is a sign of interspecific competition and characteristic for adaptive radiations.     

The evolutionary diversification of seed size: using the past to understand the present

The Devonian origin of seed plants and subsequent morphological diversification of seeds during the late Paleozoic represents an adaptive radiation into unoccupied ecological niche space. A plant's seed size is correlated with its life-history strategy, growth form, and seed dispersal syndrome. The fossil record indicates that the oldest seed plants had relatively small seeds, but the Mississippian seed size envelope increased significantly with the diversification of larger seeded lineages. Fossil seeds equivalent to the largest extant gymnosperm seeds appeared by the Pennsylvanian, concurrent with morphological diversification of growth forms and dispersal syndromes as well as the clade's radiation into new environments. Wang's Analysis of Skewness indicates that the evolutionary trend of increasing seed size resulted from primarily passive processes in Pennsylvanian seed plants. The distributions of modern angiosperms indicate a more diverse system of active and some passive processes, unbounded by Paleozoic limits; multiple angiosperm lineages independently evolved though the upper and lower bounds. Quantitative measures of preservation suggest that, although our knowledge of Paleozoic seeds is far from complete, the evolutionary trend in seed size is unlikely to be an artifact of taphonomy.     

Rapid lineage accumulation in a non-adaptive radiation: phylogenetic analysis of diversification rates in eastern North American woodland salamanders (Plethodontidae: Plethodon)

Adaptive radiations have served as model systems for quantifying the build-up of species richness. Few studies have quantified the tempo of diversification in species-rich clades that contain negligible adaptive disparity, making the macroevolutionary consequences of different modes of evolutionary radiation difficult to assess. We use mitochondrial-DNA sequence data and recently developed phylogenetic methodologies to explore the tempo of diversification of eastern North American Plethodon, a species-rich clade of woodland salamanders exhibiting only limited phenotypic disparity. Lineage-through-time analysis reveals a high rate of lineage accumulation, 0.8 species per million years, occurring 11-8 million years ago in the P. glutinosus species group, followed by decreasing rates. This high rate of lineage accumulation is exceptional, comparable to the most rapid of adaptive radiations. In contrast to classic models of adaptive radiation where ecological niche divergence is linked to the origin of species, we propose that phylogenetic niche conservatism contributes to the rapid accumulation of P. glutinosus-group lineages by promoting vicariant isolation and multiplication of species across a spatially and temporally fluctuating environment. These closely related and ecologically similar lineages persist through long-periods of evolutionary time and form strong barriers to the geographic spread of their neighbours, producing a subsequent decline in lineage accumulation. Rapid diversification among lineages exhibiting long-term maintenance of their bioclimatic niche requirements is an under-appreciated phenomenon driving the build-up of species richness.     

Diversification rates have no effect on the convergent evolution of foraging strategies in the most speciose genus of bats,Myotis*

Adaptive radiations are defined as rapid diversification with phenotypic innovation led by colonization to new environments. Notably, adaptive radiations can occur in parallel when habitats with similar selective pressures are accessible promoting convergent adaptions. Although convergent evolution appears to be a common process, it is unclear what are the main drivers leading the reappearance of morphologies or ecological roles. We explore this question in Myotis bats, the only Chiropteran genus with a worldwide distribution. Three foraging strategies—gleaning, trawling, and aerial netting—repeatedly evolved in several regions of the world, each linked to characteristic morphologies recognized as ecomorphs. Phylogenomic, morphometric, and comparative approaches were adopted to investigate convergence of such foraging strategies and skull morphology as well as factors that explain diversification rates. Genomic and morphometric data were analyzed from ～80% extant taxa. Results confirm that the ecomorphs evolved multiple times, with trawling evolving more often and foliage gleaning most recently. Skull morphology does not reflect common ancestry and evolves convergently with foraging strategy. Although diversification rates have been roughly constant across the genus, speciation rates are area‐dependent and higher in taxa with temperate distributions. Results suggest that in this species‐rich group of bats, first, stochastic processes have led divergence into multiple lineages. Then, natural selection in similar niches has promoted repeated adaptation of phenotypes and foraging strategies. Myotis bats are thus a remarkable case of ecomorphological convergence and an emerging model system for investigating the genomic basis of parallel adaptive radiation.     

Phylogenetic evidence from freshwater crayfishes that cave adaptation is not an evolutionary dead‐end

Caves are perceived as isolated, extreme habitats with a uniquely specialized biota, which long ago led to the idea that caves are “evolutionary dead‐ends.” This implies that cave‐adapted taxa may be doomed for extinction before they can diversify or transition to a more stable state. However, this hypothesis has not been explicitly tested in a phylogenetic framework with multiple independently evolved cave‐dwelling groups. Here, we use the freshwater crayfish, a group with dozens of cave‐dwelling species in multiple lineages, as a system to test this hypothesis. We consider historical patterns of lineage diversification and habitat transition as well as current patterns of geographic range size. We find that while cave‐dwelling lineages have small relative range sizes and rarely transition back to the surface, they exhibit remarkably similar diversification patterns to those of other habitat types and appear to be able to maintain a diversity of lineages through time. This suggests that cave adaptation is not a “dead‐end” for freshwater crayfish, which has positive implications for our understanding of biodiversity and conservation in cave habitats.     

Dealing with incomplete taxon sampling and diversification of a large clade of mushroom-forming fungi

The absence of an adequate fossil record can hinder understanding the process of diversification that underlies the evolutionary history of a given group. In such cases, investigators have used ultrametric trees derived from molecular data from extant taxa to gain insights into processes of speciation and extinction over time. Inadequate taxon sampling, however, impairs such inferences. In this study, we use simulations to investigate the effect of incomplete taxon sampling on the accumulation of lineages through time for a clade of mushroom-forming fungi, the Hebelomateae. To achieve complete taxon sampling, we use a new Bayesian approach that incorporates substitute lineages to estimate diversification rates. Unlike many studies of animals and plants, we find no evidence of a slowdown in speciation. This indicates the Hebelomateae has not undergone an adaptive radiation. Rather, these fungi have evolved under a relatively constant rate of diversification since their most recent common ancestor, which we date back to the Eocene. The estimated net diversification rate (0.08-0.19 spp./lineage/Ma) is comparable with that of many plants and animals. We suggest that continuous diversification in the Hebelomateae has been facilitated by climatic and vegetation changes throughout the Cenozoic. We also caution against modeling multiple genes as a single partition when performing phylogenetic dating analyses.     

Inter- and intra-morph patterns in helminth communities of sympatric whitefish morphs

Infection patterns of trophically transmitted helminth parasites were compared with feeding ecology in two sympatric whitefish Coregonus lavaretus morphs from two lake systems in northern Norway. In both lakes, the pelagic morph was an obligate zooplanktivore, while the benthic morph utilized both the benthivore and zooplanktivore trophic niches. The differences in niche utilization between the two morphs were associated with differences in trophic morphology (gill raker numbers), suggesting that they were genetically dissimilar and reproductively isolated. The benthic morph had the highest number of helminth species, probably because they exhibited a broader niche width compared to the pelagic morph. In both lakes, the species composition and intensities of helminths reflected the trophic diversification of the whitefish ecotypes with respect to different habitat choice (benthic v . pelagic) and dietary specialization (benthivore v . zooplanktivore feeding strategies within the benthic whitefish morph). Zooplanktivorous fish from both morphs acquired parasites mainly from pelagic copepods and in almost equal quantities. The benthivore feeders within the benthic morph had the highest proportion of parasites with transmission stages from benthic organisms. Host feeding behaviour seemed to be a major determinant of the helminth community structure, and helminths appeared to be useful indicators of long-term trophic specialization of whitefish ecotypes.     

Out of the dark: 350 million years of conservatism and evolution in diel activity patterns in vertebrates

Many animals are active only during a particular time (e.g., day vs. night), a partitioning that may have important consequences for species coexistence. An open question is the extent to which this diel activity niche is evolutionarily conserved or labile. Here, we analyze diel activity data across a phylogeny of 1914 tetrapod species. We find strong phylogenetic signal, showing that closely related species tend to share similar activity patterns. Ancestral reconstructions show that nocturnality was the most likely ancestral diel activity pattern for tetrapods and many major clades within it (e.g., amphibians, mammals). Remarkably, nocturnal activity appears to have been maintained continuously in some lineages for ～350 million years. Thus, we show that traits involved in local‐scale resource partitioning can be conserved over strikingly deep evolutionary time scales. We also demonstrate a potentially important (but often overlooked) metric of niche conservatism. Finally, we show that diurnal lineages appear to have faster speciation and diversification rates than nocturnal lineages, which may explain why there are presently more diurnal tetrapod species even though diurnality appears to have evolved more recently. Overall, our results may have implications for studies of community ecology, species richness, and the evolution of diet and communication systems.     

Why do leafcutter bees cut leaves? New insights into the early evolution of bees

Stark contrasts in clade species diversity are reported across the tree of life and are especially conspicuous when observed in closely related lineages. The explanation for such disparity has often been attributed to the evolution of key innovations that facilitate colonization of new ecological niches. The factors underlying diversification in bees remain poorly explored. Bees are thought to have originated from apoid wasps during the Mid-Cretaceous, a period that coincides with the appearance of angiosperm eudicot pollen grains in the fossil record. The reliance of bees on angiosperm pollen and their fundamental role as angiosperm pollinators have contributed to the idea that both groups may have undergone simultaneous radiations. We demonstrate that one key innovation--the inclusion of foreign material in nest construction--underlies both a massive range expansion and a significant increase in the rate of diversification within the second largest bee family, Megachilidae. Basal clades within the family are restricted to deserts and exhibit plesiomorphic features rarely observed among modern bees, but prevalent among apoid wasps. Our results suggest that early bees inherited a suite of behavioural traits that acted as powerful evolutionary constraints. While the transition to pollen as a larval food source opened an enormous ecological niche for the early bees, the exploitation of this niche and the subsequent diversification of bees only became possible after bees had evolved adaptations to overcome these constraints.     

Shifts in Climate Foster Exceptional Opportunities for Species Radiation: The Case of South African Geraniums

Climate change is often assumed to be a major driver of biodiversity loss. However, it can also set the stage for novel diversification in lineages with the evolutionary ability to colonize new environments. Here we tested if the extraordinary evolutionary success of the genus Pelargonium was related to the ability of its species to capitalize on the climate niche variation produced by the historical changes in southern Africa. We evaluated the relationship between rates of climate niche evolution and diversification rates in the main Pelargonium lineages and disentangled the roles of deep and recent historical events in the modification of species niches. Pelargonium clades exhibiting higher ecological differentiation along summer precipitation (SPP) gradients also experienced higher diversification rates. Faster rates of niche differentiation in spatially structured variables, along with lower levels of niche overlap among closely related species, suggest recent modification in species niches (e.g. dispersal or range shift) and niche lability. We suggest that highly structured SPP gradients established during the aridification process within southern Africa, in concert with niche lability and low niche overlap, contributed to species divergence. These factors are likely to be responsible for the extensive diversification of other lineages in this diversity hot spot.     

A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae)

The Antarctic fish family Nototheniidae (Perciformes) presumably originated from a benthic ancestor, and several lineages have evolved to live or at least feed in the water column, a trend called pelagization. Here, we use information on phylogeny, allometric growth, and diet composition for an integrated analysis of morphological and ecological diversification in this group, mainly focusing on the subfamilies Trematominae and Pleuragramminae. A phylogenetic analysis of data published in earlier systematic studies produced eight equally parsimonious trees, all indicating that several previously recognized taxa are paraphyletic. These phylogenetic trees all suggest multiple origins of pelagic life styles. Multivariate morphometric analyses including nine species showed that juveniles and adults grow according to a common pattern of ontogenetic allometry. The morphometric differences among species are mosdy the result of lateral transpositions of the growth trajectories, indicating that embryonic and larval development is more important as a determinant of morphological variation than allometric growth as juveniles and adults. We studied patterns of interspecific variation with principal components and the covariation between morphometric variables and food composition with a partial least-squares analysis. Both analyses revealed a gradient from benthic to pelagic foragers. Measurements of structures involved in swimming have a prominent role in these analyses, suggesting adaptive evolution of these traits. Tracing morphometric traits on the phylogenetic trees revealed a considerable amount of evolutionary plasticity, showing that species related phylogenetically need not be morphologically similar, but can diverge considerably, perhaps as a response to natural selection and adaptation to different habitats and foraging modes. In accordance, a test of phylogenetically independent contrasts showed that bursts of increased morphological change accompanied habitat shifts.     

LIVE-BIRTH IN VIPERS (VIPERIDAE) IS A KEY INNOVATION AND ADAPTATION TO GLOBAL COOLING DURING THE CENOZOIC

The identification of adaptations and key innovations has long interested biologists because they confer on organisms the ability to exploit previously unavailable ecological resources and respond to novel selective pressures. Although it can be extremely difficult to test for the effects of a character on the rate of lineage diversification, the convergent evolution of a character in multiple lineages provides an excellent opportunity to test for the effect of that character on lineage diversification. Here, I examine the effect of parity mode on the diversification of vipers, which have independently evolved viviparity in at least 13 lineages. I find strong statistical evidence that viviparous species diversify at a greater rate than oviparous species and correlate major decreases in the diversification rate of oviparous species with periods of global cooling, such as the Oligocene. These results suggest that the evolution of viviparity buffered live-bearing species against the negative effects of global climate change during the Cenozoic, and was a key innovation in the evolution and diversification of live-bearing vipers.     

Niche divergence and lineage diversification among closely related Sistrurus rattlesnakes

Comparing niche divergence among closely related taxa can yield important insights into the ecological distinctiveness of genetically similar forms, and identify the processes that are responsible for diversification in such organisms. Here, we apply newly developed techniques for analysing niche divergence to assess how ecologically distinct a group of closely related rattlesnakes (Sistrurus sp.) are and to explore the role that niche divergence may have played in their diversification. We find that all taxa even the most recently evolved subspecies (approximately 100,000 years old) are now ecologically distinct, implying a role for ecology in the diversification process. Statistical analysis based on comparisons with null models show that niche divergence between forms is more common than niche conservation. Finally, there is nonlinear relationship between phylogenetic and niche divergence in this group whereby niche divergence develops more rapidly between recently diverged subspecies than more distantly related forms. Overall, our results argue that ecology may play an important role in the diversification process in these snakes.     

Repeated evolution and reversibility of self‐fertilization in the volvocine green algae*

Outcrossing and self‐fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self‐fertilization is thought to be an evolutionary “dead‐end” strategy, beneficial in the short term but costly in the long term, resulting in self‐fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self‐fertilization. We use ancestral‐state reconstructions to show that self‐fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self‐fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self‐fertilization as a dead‐end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self‐fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self‐fertilization (i.e., non‐tippy distribution, no decreased diversification rates) may be explained by the haploid‐dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.     

Rapid increase in snake dietary diversity and complexity following the end-Cretaceous mass extinction

The Cenozoic marked a period of dramatic ecological opportunity in Earth history due to the extinction of non-avian dinosaurs as well as to long-term physiographic changes that created new biogeographic theaters and new habitats. Snakes underwent massive ecological diversification during this period, repeatedly evolving novel dietary adaptations and prey preferences. The evolutionary tempo and mode of these trophic ecological changes remain virtually unknown, especially compared with co-radiating lineages of birds and mammals that are simultaneously predators and prey of snakes. Here, we assemble a dataset on snake diets (34,060 observations on the diets of 882 species) to investigate the history and dynamics of the multidimensional trophic niche during the global radiation of snakes. Our results show that per-lineage dietary niche breadths remained remarkably constant even as snakes diversified to occupy disparate outposts of dietary ecospace. Rapid increases in dietary diversity and complexity occurred in the early Cenozoic, and the overall rate of ecospace expansion has slowed through time, suggesting a potential response to ecological opportunity in the wake of the end-Cretaceous mass extinction. Explosive bursts of trophic innovation followed colonization of the Nearctic and Neotropical realms by a group of snakes that today comprises a majority of living snake diversity. Our results indicate that repeated transformational shifts in dietary ecology are important drivers of adaptive radiation in snakes and provide a framework for analyzing and visualizing the evolution of complex ecological phenotypes on phylogenetic trees.

The Cenozoic marked a period of dramatic ecological opportunity in Earth history due to the extinction of non-avian dinosaurs and long-term physiographic changes. This phylogenetic natural history study offers new insights into the evolution of snake ecological diversity after the end-Cretaceous mass extinction, as they took advantage of these new opportunities.     

Pleistocene glacial cycles drove lineage diversification and fusion in the Yosemite toad (Anaxyrus canorus)

Species endemic to alpine environments can evolve via steep ecological selection gradients between lowland and upland environments. Additionally, many alpine environments have faced repeated glacial episodes over the past two million years, fracturing these endemics into isolated populations. In this “glacial pulse” model of alpine diversification, cycles of allopatry and ecologically divergent glacial refugia play a role in generating biodiversity, including novel admixed (“fused”) lineages. We tested for patterns of glacial pulse lineage diversification in the Yosemite toad (Anaxyrus [Bufo] canorus), an alpine endemic tied to glacially influenced meadow environments. Using double‐digest RADseq on populations densely sampled from a portion of the species range, we identified nine distinct lineages with divergence times ranging from 18 to 724 thousand years ago (ka), coinciding with multiple Sierra Nevada glacial events. Three lineages have admixed origins, and demographic models suggest these fused lineages have persisted throughout past glacial cycles. Directionality indices supported the hypothesis that some lineages recolonized Yosemite from east of the ice sheet, whereas other lineages remained in western refugia. Finally, refugial niche reconstructions suggest that low‐ and high‐elevation lineages have convergently adapted to similar climatic niches. Our results suggest glacial cycles and refugia may be important crucibles of adaptive diversity across deep evolutionary time.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.     

Larval habits, host-plant associations, and speciation in nematine sawflies (Hymenoptera: Tenthredinidae)

Adaptive radiations consist of two intertwined processes, diversification of species and diversification of their ecological niches, but it is unclear whether there is a causal link between the processes. In phytophagous insects, ecological diversification mainly involves shifts in host-plant associations and in larval feeding habits (internal or external) on different plant parts, and several observations indicate that speciation is facilitated by host shifts. Data on host use in individual species suggest that internal feeders are less likely to colonize new hosts than external-feeding taxa and, consequently, increases in collective host ranges and species numbers should be slowed down in endophagous lineages. We tested these related hypotheses by using phylogenetic information to reconstruct the evolutionary history of larval resource use in the sawfly subfamily Nematinae, a group of 1000 plus species with a broad range of niches: the subfamily's combined host range includes over 20 plant families, and larvae may feed externally on leaves or needles, or internally, for example, in buds, fruits, leaves, or galls. The results show that: (1) Most internally feeding groups have evolved independently from external-feeding ancestors, but several distinct internal habits have appeared convergently multiple times; (2) Shifts among host taxa are clearly more common than changes in larval habits; (3) The majority of host switches have occurred among phylogenetically close plant groups, but many shifts are manifest among distantly related, ecologically proximate hosts; (4) Although external feeding characteristic of the common ancestor of Nematinae is associated with relatively high rates of host-shifting, internal feeders are very conservative in their host use; (5) In contrast, the effect of endophagy on speciation probabilities is more variable: net speciation rates are lowered in most internal-feeding groups, but a striking exception is found in species that induce galls on Salicaceae. The loose connection between collective host ranges and species diversity provides empirical support for theoretical models suggesting that speciation rates are a function of a complex interplay between "intrinsic" niche width and resource heterogeneity.