Thomas J. Firneno, Corey E. Roelke, A. Leaché, Nathan D. Rains, Toby J. Hibbitts, Wade Ryberg, Travis Laduc, Sonal Singhal, Matthew Fujita
{"title":"Genome-wide Data Reinforces the Evolutionary Relationships of Previously Problematic Earless Lizards (Phyrnosomatidae: Holbrookia)","authors":"Thomas J. Firneno, Corey E. Roelke, A. Leaché, Nathan D. Rains, Toby J. Hibbitts, Wade Ryberg, Travis Laduc, Sonal Singhal, Matthew Fujita","doi":"10.18061/bssb.v3i2.9459","DOIUrl":"https://doi.org/10.18061/bssb.v3i2.9459","url":null,"abstract":"In the face of anthropogenic change and the potential loss of species, documenting biodiversity – including accurately delimiting species complexes – is of tantamount importance. Genome-wide data are powerful for investigating lineage divergence, though deciding if this divergence represents species-level differentiation remains challenging. Here, we use genome-wide data to investigate species limits in four currently recognized species of Earless Lizards (Phrynosomatidae: Holbrookia), with a focus on H. lacerata and H. subcaudalis, the latter having potentially imperiled populations. This group’s taxonomy has been repeatedly revised; most recently, H. lacerata and H. subcaudalis were elevated to species status using conserved morphological data and a few molecular markers. In this study, we used double-digest restriction-site associated DNA sequencing to delineate species limits for our focal taxa. We recovered five populations that corresponded to five well-supported lineages with very little gene flow among them. Our results support the recognition of H. lacerata and H. subcaudalis as two separate species, based on strong phylogenetic support for these lineages and genetic divergence measures that exceed those of currently recognized species within Holbrookia. Genomic methods for species delimitation offer a promising approach to assess biodiversity in taxonomically confounded taxa or organisms of conservation priority.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"122 36","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-07-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141657052","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Lennart J. J. van de Peppel, Wilhelm De Beer, N. Koné, Duur Aanen
{"title":"Species and Speciation in the Termite-Cultivated Fungus Termitomyces","authors":"Lennart J. J. van de Peppel, Wilhelm De Beer, N. Koné, Duur Aanen","doi":"10.18061/bssb.v3i2.9345","DOIUrl":"https://doi.org/10.18061/bssb.v3i2.9345","url":null,"abstract":"Termitomyces is a genus of basidiomycete fungi cultivated by termites of the subfamily Macrotermitinae. This symbiosis originated in central Africa, and subsequently, the fungus-growing termites have colonized almost the entire African continent including Madagascar as well as significant parts of Asia. Around 40 species of Termitomyces have been described based on morphology of the sexual fruit bodies, which are associated with some 330 species of fungus-growing termites distributed over 11 genera. However, the total number of fungal species may be higher as not all species regularly produce mushrooms, and morphological variation does not seem to be a reliable criterion for species delimitation in this group. In this study we estimated the total number of species based on ITS-barcode criteria and assessed host specificity and geographic differentiation to infer patterns of speciation. We estimated the total number of phylogenetic species using two methods of DNA sequence-based species delimitation; Automatic Barcode Gap Discovery (ABGD) and the Generalized Mixed Yule Coalescent (GMYC) model on a large dataset of over 1,500 ITS sequences from laboratory cultures, fungarium specimens and the public database NCBI Genbank. This resulted in an estimated 87 species hypotheses using ABGD and 94 species hypotheses using the GMYC model. A phylogenetic reconstruction was performed on representative sequences of the 87 species hypotheses identified by ABGD (the most conservative estimate) constrained by a well-supported phylogeny based on whole-genome data to address host specificity and geographical differentiation. Five main clades were recovered which generally were associated with species of one or two host genera, except for samples collected from the genera Microtermes and Ancistrotermes, which formed two separate non-sister clades. We did not find any evidence for long-term host fidelity as would be expected for species with strict uniparental vertical symbiont transmission. We found strict geographic separation between African and Asian species of Termitomyces and infer a minimum of seven inter-continental migrations. We show that epigeous fruiting of the T. microcarpus group has a single evolutionary origin in Africa and that fruiting in species of this group likely is induced by the fungus rather than by the host-termite species. In contrast, fruiting in the symbionts of some species of Microtermes and Macrotermes may be suppressed by the host-termite species, since mushrooms of certain fungal species are found when those species are associated with some termite-host genera, but never when associated with other host genera. We discuss some examples of incongruence between morphological and phylogenetic species concepts and give suggestions to improve the taxonomy of the genus Termitomyces.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"3 2","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-07-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141661559","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Blake Fauskee, Andrew Crowl, Bryan Piatkowski, Anne Yoder, G. Tiley
{"title":"Ancient Introgression in Mouse Lemurs (Microcebus: Cheirogaleidae) Explains 20 Years of Phylogenetic Uncertainty","authors":"Blake Fauskee, Andrew Crowl, Bryan Piatkowski, Anne Yoder, G. Tiley","doi":"10.18061/bssb.v3i1.9319","DOIUrl":"https://doi.org/10.18061/bssb.v3i1.9319","url":null,"abstract":"Mouse lemurs (genus Microcebus) are a clade of approximately 26 named species of small, nocturnal primates endemic to Madagascar. The genus radiated one to ten million years ago and is morphologically cryptic, with most species having been named within the past 20 years largely based on phylogenetic analysis of short fragments of mitochondrial data. More recent work has been focused on revisiting species designations with autosomal nuclear data using more sophisticated statistical approaches. The order of speciation events in Microcebus remains contentious, particularly with regard to the placement of the M. ravelobensis clade. We investigated support for previous phylogenetic hypotheses based on available whole-genome assemblies from six species and an outgroup. We recovered over 4,000 one-to-one orthologs from these assemblies and used concatenation and coalescent species tree methods to evaluate if differences between previous studies were due to methodological differences or to limitations from too few loci. Observed gene tree discordance was high with patterns inconsistent with incomplete lineage sorting alone. Therefore, we estimated phylogenetic networks to investigate ancient introgression events that may explain observed gene tree distributions and previous phylogenetic conflicts. A network model, invoking some role for introgressive hybridization in the early evolution of Microcebus, better characterizes phylogenetic relationships than does any binary species tree. Our results provide insights into the biogeographic history of a threatened and diverse group of primates while also highlighting an important role for phylogenetic network methods in resolving cases of phylogenetic uncertainty.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"9 13","pages":""},"PeriodicalIF":0.0,"publicationDate":"2024-07-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141685182","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Basanta Khakurel, Zachary L. Nikolakis, B. Crother, April Wright
{"title":"Species Delimitation of Eastern Pinesnake Complex (Pituophis melanoleucus)","authors":"Basanta Khakurel, Zachary L. Nikolakis, B. Crother, April Wright","doi":"10.18061/bssb.v2i1.9423","DOIUrl":"https://doi.org/10.18061/bssb.v2i1.9423","url":null,"abstract":"The eastern Pinesnake (Pituophis melanoleucus) is found throughout eastern United States. Taxonomy in this group has been controversial with several conflicting species designations. Three subspecies of the eastern Pinesnake have prevailed in the literature to their geographic locations and scale coloration: the northern Pinesnake (P. m. melanoleucus), the Florida Pinesnake (P. m. mugitus), and the Black Pinesnake (P. m. lodingi). Within the region, there are several major barriers to dispersal, particularly major river drainage systems and human modification of the longleaf pine habitat. Consistently, a lack of phylogenetic resolution has plagued these taxa in prior studies. The goal of this study was to examine the taxonomic validity of the eastern Pinesnake complex using single nucleotide polymorphisms (SNPs) isolated from ultra-conserved elements (UCEs) in phylogenetic and population genetic approaches. Molecular species delimitation approaches indicated that the population of eastern Pinesnake exhibits population structure across its range that may rise to the level of being new species.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"6 7","pages":""},"PeriodicalIF":0.0,"publicationDate":"2023-12-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138944154","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The Species as a Reproductive Community Emerging From the Past","authors":"W. Maddison, Jeannette Whitton","doi":"10.18061/bssb.v2i1.9358","DOIUrl":"https://doi.org/10.18061/bssb.v2i1.9358","url":null,"abstract":"Biologists and philosophers of science have been unable to fully resolve the decades-long controversy as to what kind of unit of living biodiversity should receive the valued label “species”: reproductive communities (among sexual organisms), genealogical groups, or clusters of organisms that share traits. Among these choices, which represent a spectrum from process to history to observable outcome (respectively), the latter (more operationalist) concepts are not viable. Species of sexual organisms must embody or imply cohesive and integrating processes such as interbreeding and shared ecological pressures if they are to have sufficient power to bear the burden we give them: to predict or explain traits across the genome and among organisms. This commitment to cohesive process is needed whether biologists use species as taxonomic containers to synthesize data, as minimal phylogenetic units, or as actors in evolutionary diversification. These varied uses can be satisfied via a concept of reproductive community, but not the strict Biological Species Concept (BSC). Its two drawbacks are a focus on the contemporary and a restriction to intrinsic factors. Current reproductive compatibility may predict future matings, but it does not explain well the traits and genes that living organisms already have. The organisms alive today were shaped by isolating factors of the past, not those of the present, to whatever extent those differ. The most broadly-useful species concept must therefore see species retrospectively, as reproductive communities of the past. As well, the BSC’s exclusion of extrinsic factors renders each of its units incomplete in explanation and synthesis. Reproductive communities in nature were isolated not just by intrinsic (genetic) differences, but also by purely extrinsic (e.g., geographic) factors. Such reproductive communities were and are real, natural entities whose integrated and self-reinforcing cohesive processes constrained genealogical descent and aligned the distribution of many traits. This Retrospective Reproductive Community Concept (RRCC), formalized mathematically in multispecies coalescent models, justifies the traditional practice of taxonomists using morphological data to seek the echoes of past reproductive cohesion. However, which reproductive communities naturally deserve to be ranked as species, and which as demes or populations, is a vexing question. There is no natural, discrete and broadly informative species rank that applies universally, or perhaps even usually. To whatever extent species rank is justified, it is as justified for asexual organisms as for sexuals. The presence or absence of sex is just one example of the variability biologists confront. Because cohesive processes vary among clades, a useful and broadly-applicable species concept cannot specify detailed cohesive mechanisms. Nor can it perfectly align the named species of taxonomy with units of evolution, because the latter are not structured to","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"57 3","pages":""},"PeriodicalIF":0.0,"publicationDate":"2023-12-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"138588054","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Benjamin Teo, Jeffrey Rose, Paul Bastide, Cécile Ané
{"title":"Accounting for Within-Species Variation in Continuous Trait Evolution on a Phylogenetic Network","authors":"Benjamin Teo, Jeffrey Rose, Paul Bastide, Cécile Ané","doi":"10.18061/bssb.v2i3.8977","DOIUrl":"https://doi.org/10.18061/bssb.v2i3.8977","url":null,"abstract":"Within-species trait variation may be the result of genetic variation, environmental variation, or measurement error, for example. In phylogenetic comparative studies, failing to account for within-species variation has many adverse effects, such as increased error in testing hypotheses about evolutionary correlations, biased estimates of evolutionary rates, and inaccurate inference of the mode of evolution. These adverse effects were demonstrated in studies that considered a tree-like underlying phylogeny. Comparative methods on phylogenetic networks are still in their infancy. The impact of within-species variation on network-based methods has not been studied. Here, we introduce a phylogenetic linear model in which the phylogeny can be a network to account for within-species variation in the continuous response trait assuming equal within-species variances across species. We show how inference based on the individual values can be reduced to a problem using species-level summaries, even when the within-species variance is estimated. Our method performs well under various simulation settings and is robust when within-species variances are unequal across species. When phenotypic (within-species) correlations differ from evolutionary (between-species) correlations, estimates of evolutionary coefficients are pulled towards the phenotypic coefficients for all methods we tested. Also, evolutionary rates are either underestimated or overestimated, depending on the mismatch between phenotypic and evolutionary relationships. We applied our method to morphological and geographical data from Polemonium. We find a strong negative correlation of leaflet size with elevation, despite a positive correlation within species. Our method can explore the role of gene flow in trait evolution by comparing the fit of a network to that of a tree. We find marginal evidence for leaflet size being affected by gene flow and support for previous observations on the challenges of using individual continuous traits to infer inheritance weights at reticulations. Our method is freely available in the Julia package PhyloNetworks.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"143 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135823637","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sungsik Kong, Santiago J. Sánchez-Pacheco, Robert Murphy
{"title":"Median-Joining Networks and Bayesian Phylogenies Often Do Not Tell the Same Story","authors":"Sungsik Kong, Santiago J. Sánchez-Pacheco, Robert Murphy","doi":"10.18061/bssb.v2i1.9625","DOIUrl":"https://doi.org/10.18061/bssb.v2i1.9625","url":null,"abstract":"Inferring phylogenies among intraspecific individuals often yields unresolved relationships (i.e., polytomies). Consequently, methods that compute distance-based abstract networks, like Median-Joining Networks (MJNs), are thought to be more appropriate tools for reconstructing such relationships than traditional trees. Median-Joining Networks visualize all routes of relationships in the form of cycles, if needed, when traditional approaches cannot resolve them. However, the MJN method is a distance-based phenetic approach that does not involve character transformations and makes no reference to ancestor–descendant relationships. Although philosophical and theoretical arguments challenging the implication that MJNs reflect phylogenetic signal in the traditional sense have been presented elsewhere, an empirical comparison with a character-based approach is needed given the increasing popularity of MJN analysis in evolutionary biology. Here, we use the conservative Approximately Unbiased (AU) test to compare 85 cases of branching patterns of cycle-free MJNs and Bayesian Inference (BI) phylogenies using datasets from 55 empirical studies. By rooting the MJN analyses to provide directionality, we report substantial disagreement between computed MJNs and posterior distributions on BI phylogenies. The branching patterns in MJNs and BI phylogenies show significantly different relationships in 37.6% of cases. Among the relationships that do not significantly differ, 96.2% show alternative sets of relationships. Our results indicate that the two methods provide different measures of relatedness in a phylogenetic sense. Finally, our analyses also support previous observations of the statistical hypothesis testing by reconfirming the over-conservativeness of the Shimodaira-Hasegawa test versus the AU test.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"49 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136098195","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Perspectives on the Grey Zone of Species Delimitation With Notes on Invertebrates in the Marine Environment","authors":"Catalina Ramírez-Portilla, Andrea M. Quattrini","doi":"10.18061/bssb.v2i2.9255","DOIUrl":"https://doi.org/10.18061/bssb.v2i2.9255","url":null,"abstract":"Defining species boundaries, or delimiting species, is a complex and often difficult task. Indeed, when such studies incorporate approaches that consider evolutionary mechanisms, there is much to be learned about species diversity and how the processes that play critical roles in speciation can impact species delineation. In 2021, a virtual workshop on species delimitation was held at the Smithsonian Institution National Museum of Natural History to train natural history scientists and taxonomists on the appropriate analytical tools that can be used to help delimit species when using molecular data. This perspective highlights some of the main themes discussed during that workshop while detailing three processes that can challenge any species delimitation study. Specifically, we discuss incomplete lineage sorting, gene flow, and population structure when delimiting species boundaries using molecular data. We highlight empirical studies and methodological approaches that have successfully met these challenges under various scenarios. Finally, we provide recommendations and considerations for undertaking species delimitation studies in a variety of taxa. To this end, we recommend that taxonomists fully embrace process-based species delimitation, which can provide important insights into speciation in their study systems. For those developing analytical approaches, we hope they consider incorporating less well-known taxa, such as marine invertebrates, into method testing. Marine invertebrates encompass many dark taxa across the tree of life yet represent the majority of animal phyla, many of which are vulnerable to extinction due to global ocean change. Thus, advancing species delimitation to address taxonomic revisions in these organisms will support conservation decisions on keystone ecosystems. Furthermore, the diversity of their life history strategies, the lack of obvious barriers to gene flow in the ocean environment, and their occurrence in isolated habitat patches can better inform our knowledge of speciation and the evolutionary processes that play a role in generating diversity in nature.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"49 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135591382","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Justin M. Bernstein, Hugo De Souza, John Murphy, Harold Voris, Rafe Brown, Edward Myers, Sean Harrington, Kartik Shanker, Sara Ruane
{"title":"Phylogenomics of Fresh and Formalin Specimens Resolves the Systematics of Old World Mud Snakes (Serpentes: Homalopsidae) and Expands Biogeographic Inference","authors":"Justin M. Bernstein, Hugo De Souza, John Murphy, Harold Voris, Rafe Brown, Edward Myers, Sean Harrington, Kartik Shanker, Sara Ruane","doi":"10.18061/bssb.v2i1.9393","DOIUrl":"https://doi.org/10.18061/bssb.v2i1.9393","url":null,"abstract":"Our knowledge of the biodiversity of Asia and Australasia continues to expand with more focused studies on systematics of various groups and their biogeography. Historically, fluctuating sea levels and cyclic connection and separation of now-disjunct landmasses have been invoked to explain the accumulation of biodiversity via species pump mechanisms. However, recent research has shown that geological shifts of the mainland and species dispersal events may be better explanations of the biodiversity in these regions. We investigate these processes using the poorly studied and geographically widespread Mud Snakes (Serpentes: Homalopsidae) using a target capture approach of ~4,800 nuclear loci from fresh tissues and supplemental mitochondrial data from formalin tissues from museum specimens. We use these datasets to reconstruct the first resolved phylogeny of the group, identify their biogeographic origins, and test hypotheses regarding the roles of sea-level change and habitat selection on their diversification. Divergence dating and ancestral range estimation yielded support for an Oligocene origin and diversification from mainland Southeast Asia and Sundaland in the rear-fanged group ~20 million years ago, followed by eastward and westward dispersal. GeoHiSSE models indicate that niche expansion of ancestral, rear-fanged lineages into aquatic environments did not impact their diversification rates. Our results highlight that Pleistocene sea-level changes and habitat specificity did not primarily lead to the extant species richness of Homalopsidae and that, alternatively, geological shifts in mainland Southeast Asia may have been a major driver of diversity in this group. We also emphasize the importance of using fresh and degraded tissues, and both nuclear and mitochondrial DNA, for filling knowledge gaps in poorly known but highly diverse and conceptually important groups. Here, Homalopsidae represents a non-traditional but effective model study system for understanding transitions between terrestrial, marine, and freshwater environments.","PeriodicalId":476538,"journal":{"name":"Bulletin of the Society of Systematic Biologists","volume":"37 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-09-13","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135690683","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":0,"RegionCategory":"","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}