skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, May 23 until 2:00 AM ET on Friday, May 24 due to maintenance. We apologize for the inconvenience.

Title: Evolutionary legacies in contemporary tetrapod imperilment

The Tree of Life will be irrevocably reshaped as anthropogenic extinctions continue to unfold. Theory suggests that lineage evolutionary dynamics, such as age since origination, historical extinction filters and speciation rates, have influenced ancient extinction patterns – but whether these factors also contribute to modern extinction risk is largely unknown. We examine evolutionary legacies in contemporary extinction risk for over 4000 genera, representing ~30,000 species, from the major tetrapod groups: amphibians, birds, turtles and crocodiles, squamate reptiles and mammals. We find consistent support for the hypothesis that extinction risk is elevated in lineages with higher recent speciation rates. We subsequently test, and find modest support for, a primary mechanism driving this pattern: that rapidly diversifying clades predominantly comprise range‐restricted, and extinction‐prone, species. These evolutionary patterns in current imperilment may have important consequences for how we manage the erosion of biological diversity across the Tree of Life.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;
Publisher / Repository:
Date Published:
Journal Name:
Ecology Letters
Medium: X Size: p. 2464-2476
["p. 2464-2476"]
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Speciation rates vary substantially across the tree of life. These rates should be linked to the rate at which population structure forms if a continuum between micro and macroevolutionary patterns exists. Previous studies examining the link between speciation rates and the degree of population formation in clades have been shown to be either correlated or uncorrelated depending on the group, but no study has yet examined the relationship between speciation rates and population structure in a young group that is constrained spatially to a single‐island system. We examine this correlation in 109 gemsnakes (Pseudoxyrhophiidae) endemic to Madagascar and originating in the early Miocene, which helps control for extinction variation across time and space. We find no relationship between rates of speciation and the formation rates of population structure over space in 33 species of gemsnakes. Rates of speciation show low variation, yet population structure varies widely across species, indicating that speciation rates and population structure are disconnected. We suspect this is largely due to the persistence of some lineages not susceptible to extinction. Importantly, we discuss how delimiting populations versus species may contribute to problems understanding the continuum between shallow and deep evolutionary processes.

    more » « less
  2. Abstract

    Despite the obstacles facing marine colonists, most lineages of aquatic organisms have colonized and diversified in freshwaters repeatedly. These transitions can trigger rapid morphological or physiological change and, on longer timescales, lead to increased rates of speciation and extinction. Diatoms are a lineage of ancestrally marine microalgae that have diversified throughout freshwater habitats worldwide. We generated a phylogenomic data set of genomes and transcriptomes for 59 diatom taxa to resolve freshwater transitions in one lineage, the Thalassiosirales. Although most parts of the species tree were consistently resolved with strong support, we had difficulties resolving a Paleocene radiation, which affected the placement of one freshwater lineage. This and other parts of the tree were characterized by high levels of gene tree discordance caused by incomplete lineage sorting and low phylogenetic signal. Despite differences in species trees inferred from concatenation versus summary methods and codons versus amino acids, traditional methods of ancestral state reconstruction supported six transitions into freshwaters, two of which led to subsequent species diversification. Evidence from gene trees, protein alignments, and diatom life history together suggest that habitat transitions were largely the product of homoplasy rather than hemiplasy, a condition where transitions occur on branches in gene trees not shared with the species tree. Nevertheless, we identified a set of putatively hemiplasious genes, many of which have been associated with shifts to low salinity, indicating that hemiplasy played a small but potentially important role in freshwater adaptation. Accounting for differences in evolutionary outcomes, in which some taxa became locked into freshwaters while others were able to return to the ocean or become salinity generalists, might help further distinguish different sources of adaptive mutation in freshwater diatoms.

    more » « less
  3. Abstract

    Traits that have arisen multiple times yet still remain rare present a curious paradox. A number of these rare traits show a distinct tippy pattern, where they appear widely dispersed across a phylogeny, are associated with short branches and differ between recently diverged sister species. This phylogenetic pattern has classically been attributed to the trait being an evolutionary dead end, where the trait arises due to some short‐term evolutionary advantage, but it ultimately leads species to extinction. While the higher extinction rate associated with a dead end trait could produce such a tippy pattern, a similar pattern could appear if lineages with the trait speciated slower than other lineages, or if the trait was lost more often that it was gained. In this study, we quantify the degree of tippiness of red flowers in the tomato family, Solanaceae, and investigate the macroevolutionary processes that could explain the sparse phylogenetic distribution of this trait. Using a suite of metrics, we confirm that red‐flowered lineages are significantly overdispersed across the tree and form smaller clades than expected under a null model. Next, we fit 22 alternative models using HiSSE(Hidden State Speciation and Extinction), which accommodates asymmetries in speciation, extinction and transition rates that depend on observed and unobserved (hidden) character states. Results of the model fitting indicated significant variation in diversification rates across the family, which is best explained by the inclusion of hidden states. Our best fitting model differs between the maximum clade credibility tree and when incorporating phylogenetic uncertainty, suggesting that the extreme tippiness and rarity of red Solanaceae flowers makes it difficult to distinguish among different underlying processes. However, both of the best models strongly support a bias towards the loss of red flowers. The best fitting HiSSEmodel when incorporating phylogenetic uncertainty lends some support to the hypothesis that lineages with red flowers exhibit reduced diversification rates due to elevated extinction rates. Future studies employing simulations or targeting population‐level processes may allow us to determine whether red flowers in Solanaceae or other angiosperms clades are rare and tippy due to a combination of processes, or asymmetrical transitions alone.

    more » « less
  4. Eaton, Deren (Ed.)
    Abstract Color polymorphism—two or more heritable color phenotypes maintained within a single breeding population—is an extreme type of intraspecific diversity widespread across the tree of life. Color polymorphism is hypothesized to be an engine for speciation, where morph loss or divergence between distinct color morphs within a species results in the rapid evolution of new lineages, and thus, color polymorphic lineages are expected to display elevated diversification rates. Multiple species in the lizard family Lacertidae are color polymorphic, making them an ideal group to investigate the evolutionary history of this trait and its influence on macroevolution. Here, we produce a comprehensive species-level phylogeny of the lizard family Lacertidae to reconstruct the evolutionary history of color polymorphism and test if color polymorphism has been a driver of diversification. Accounting for phylogenetic uncertainty with multiple phylogenies and simulation studies, we estimate an ancient origin of color polymorphism (111 Ma) within the Lacertini tribe (subfamily Lacertinae). Color polymorphism most likely evolved few times in the Lacertidae and has been lost at a much faster rate than gained. Evolutionary transitions to color polymorphism are associated with shifts in increased net diversification rate in this family of lizards. Taken together, our empirical results support long-standing theoretical expectations that color polymorphism is a driver of diversification.[Color polymorphism; Lacertidae; state-dependent speciation extinction models; trait-dependent diversification.] 
    more » « less
  5. Abstract

    The complex island archipelagoes of Wallacea and Melanesia have provided empirical data behind integral theories in evolutionary biology, including allopatric speciation and island biogeography. Yet, questions regarding the relative impact of the layered biogeographic barriers, such as deep-water trenches and isolated island systems, on faunal diversification remain underexplored. One such barrier is Wallace’s Line, a significant biogeographic boundary that largely separates Australian and Asian biodiversity. To assess the relative roles of biogeographic barriers—specifically isolated island systems and Wallace’s Line—we investigated the tempo and mode of diversification in a diverse avian radiation, Corvides (Crows and Jays, Birds-of-paradise, Vangas, and allies). We combined a genus-level data set of thousands of ultraconserved elements (UCEs) and a species-level, 12-gene Sanger sequence matrix to produce a well-resolved supermatrix tree that we leveraged to explore the group’s historical biogeography and the effects of the biogeographic barriers on their macroevolutionary dynamics. The tree is well resolved and differs substantially from what has been used extensively for past comparative analyses within this group. We confirmed that Corvides, and its major constituent clades, arose in Australia and that a burst of dispersals west across Wallace’s Line occurred after the uplift of Wallacea during the mid-Miocene. We found that dispersal across this biogeographic barrier was generally rare, though westward dispersals were two times more frequent than eastward dispersals. Wallacea’s central position between Sundaland and Sahul no doubt acted as a bridge for island-hopping dispersal out of Australia, across Wallace’s Line, to colonize the rest of Earth. In addition, we found that the complex island archipelagoes east of Wallace’s Line harbor the highest rates of net diversification and are a substantial source of colonists to continental systems on both sides of this biogeographic barrier. Our results support emerging evidence that island systems, particularly the geologically complex archipelagoes of the Indo-pacific, are drivers of species diversification. [Historical biogeography; island biogeography; Melanesia; molecular phylogenetics; state-dependent diversification and extinction.]

    more » « less