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Article

Multiple Speciation and Extinction Rate Shifts Shaped the Macro-Evolutionary History of the Genus Lycium Towards a Rather Gradual Accumulation of Species Within the Genus

by
Haikui Chen
1,*,
Kowiyou Yessoufou
2,
Xiu Zhang
1,
Shouhe Lin
3 and
Ledile Mankga
4
1
School of Biological Science and Engineering, North Minzu University, Yinchuan 750021, China
2
Department of Geography, Environmental Management and Energy Studies, University of Johannesburg, Auckland Park 2006, P.O. Box 526, Johannesburg 2092, South Africa
3
School of Mathematics and Information Science, North Minzu University, Yinchuan 750021, China
4
Department of Life and Consumer Sciences, University of South Africa, Florida 1710, South Africa
*
Author to whom correspondence should be addressed.
Diversity 2024, 16(11), 680; https://doi.org/10.3390/d16110680
Submission received: 11 August 2024 / Revised: 20 October 2024 / Accepted: 31 October 2024 / Published: 6 November 2024
(This article belongs to the Special Issue 2024 Feature Papers by Diversity’s Editorial Board Members)
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Abstract

:
The Neotropics are the most species-rich region on Earth, and spectacular diversification rates in plants are reported in plants, mostly occurring in oceanic archipelagos, making Neotropical and island plant lineages a model for macro-evolutionary studies. The genus Lycium in the Solanaceae family, originating from the Neotropics and exhibiting a unique disjunct geography across several islands, is therefore expected to experience exceptional diversification events. In this study, we aimed to quantify the diversification trajectories of the genus Lycium to elucidate the diversification events within the genus. We compiled a DNA matrix of six markers on 75% of all the species in the genus to reconstruct a dated phylogeny. Based on this phylogeny, we first revisited the historical biogeography of the genus. Then, we fitted a Compound Poisson Process on Mass Extinction Time model to investigate the following key evolutionary events: speciation rate, extinction rate, as well as mass extinction events. Our analysis confirmed that South America is the origin of the genus, which may have undergone a suite of successive long-distance dispersals. Also, we found that most species arose as recently as 5 million years ago, and that the diversification rate found is among the slowest rates in the plant kingdom. This is likely shaped by the multiple speciation and extinction rate shifts that we also detected throughout the evolutionary history of the genus, including one mass extinction at the early stage of its evolutionary history. However, both speciation and extinction rates remain roughly constant over time, leading to a gradual species accumulation over time.

1. Introduction

Taxonomically, the genus Lycium L. belongs to the family Solanaceae, subfamily Solanoideae, and the tribe Lycieae [1,2,3]. Plants in this genus are long-lived spiny shrubs and small trees, usually hermaphroditic, bearing red, fleshy, and multi-seeded berries (>10 seeds; [4]). Most of these plants are adapted to arid and sub-arid ecosystems, with a few exceptions colonizing coastal environments [1,4,5,6].
Several aspects of the genus Lycium have been actively investigated. One is the phylogenetic relationship within the genus based on DNA sequences of various genes [7,8,9] or based on high-quality single-nucleotide polymorphisms [10]. These authors reported different sizes for the genus. While Fukuda et al. [7] reported 70 species, Miller [8] estimated the size of the genus to 75 species, and some studies investigated the relationships within the genus [9]. The most recent of all supported a diversification of ~80 species within the genus [10]. Another aspect that attracts much research interest is the biogeography of the genus, grounded on the fragmented distribution of the genus across Asia, Africa, and South and North America (e.g., [10]). Also, the genus shows a disjunct geographic pattern, with most species found in the New World (South America: 30 species, southwestern North America: 21 species) and in southern Africa (17 species; [4,11,12,13,14]). Additional species are found in Eurasia (from Europe to China and Japan, ten species), Australia (one species), and across the Pacific Islands (two species). For example, the species Lycium carolinianum Walt. occurs on mainland North America, from Georgia to Florida and Texas. It is also found in the Yucatán Peninsula in Mexico and Cuba [4,11] and across the island archipelagos on Easter Island, the Ogasawara Islands, the Hawaiian Islands, French Polynesia, Tonga, and the Daitou Islands [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17].
This disjunct geographic distribution raises the question of how such geography has been shaped. To this question, two hypotheses, one championed by Symon [18] and the other by Raven and Axelrod [19], have been put forward. Symon [18] proposed that the disjunct geography of Lycium was shaped by the breakup of Gondwana and the subsequent drifting of continental masses. This hypothesis is grounded in the observation that South America and southern Africa are the two species-richest regions for the genus. If that is the case, we would expect a signature of vicariance along the phylogeny of Lycium. Therefore, we refer to Symon [18]’s hypothesis as ‘the vicariance hypotheses. More than two decades ago, Fukuda et al. [7] eliminated the vicariance hypothesis as the major evolutionary forces that may have shaped the distribution of the genus and opted for the dispersal hypothesis [7]. The second hypothesis suggests that the disjunct geography of Lycium may have been rather shaped by long-distance dispersals—we term this ‘the dispersal hypothesis’ [16]. Recently, Levin and Miller [20] demonstrated that L. carolinianum colonized the Pacific Islands from around 40 to 100 years ago through dispersal events (see also Miller et al. [21]), and that, following the dispersal, the species suffered a loss of genetic diversity.
Although the biogeography of the genus Lycium is well explored, the evolutionary processes that shaped the species accumulation within the genus (e.g., speciation and extinction rates, mass extinctions, diversification shifts, vicariance, etc.) remain unknown. Indeed, biological diversity within a lineage, and even its geography, is shaped through macro-evolutionary processes, and investigating these processes allows for a deeper understanding of both the ecological and historical forces driving the diversification within the lineage. For example, the availability of empty niches is said to promote rapid speciation events, and the frequency of these events may later decrease over time as niches are being filled [22]. As such, investigating the macro-evolutionary processes driving the diversification of a given lineage may inform us on the importance of deterministic versus stochastic forces throughout the evolutionary history of a given lineage [23,24]. Such history can be reconstructed through the phylogenetic exploration of radiation events [25,26,27,28]. The analysis of lineage splitting (diversification) revealed that an increasing diversification through time is rare, as this is reported in only very few studies (e.g., [29,30,31]). Although the phylogeny of the genus Lycium has been well studied, no study quantified the macro-evolutionary events within the genus. As a genus originated in the neotropics, we expect the analysis of the macro-evolutionary events of the genus to show an increasing diversification. This is based on the knowledge that 70% of the Neotropical clades are expanding whilst 21% are saturated and 9% are declining [32]. Indeed, four scenarios are plausible to explain the overall patterns of diversification: (i) gradual expansions, (ii) exponential expansions, (iii) saturated or asymptotic expansions, and (iv) declines in diversity. A gradual expansion is likely under constant speciation and extinction rates or through a similar increase in speciation and extinction rates. However, a lineage may show a pattern of an exponential increase in species under constant extinction and increasing speciation, or when speciation rate is constant but the extinction rate decreases. Furthermore, there is a scenario of a saturated increase when the extinction rate is constant but the speciation rate decreases, and another scenario of constant speciation and increasing extinction rates. Finally, there is a scenario of waxing and waning dynamics, which is likely to occur under constant extinction and decreasing speciation or constant speciation and increasing extinction [32].
In the present study, we aimed to quantify the prevailing diversification trajectories of the genus Lycium to elucidate the diversification events within the genus Lycium and complement what is already known about the disjunct geographic distribution of the genus.

2. Materials and Methods

2.1. Assembling the Phylogeny of Lycium

To assemble the complete phylogeny of Lycium, we used the DNA matrix of four plastid regions including trnT-trnL, trnL-F, matK, trnL, and two nuclear markers (Internal Transcriped Spacer, (ITS) and Waxy from the nuclear GBSSI gene) from Fukuda et al. [7], Levin and Miller [9], and Levin et al. [33]. Following Levin et al. [33], the monotypic genus Phrodus Miers [3] and the genus Grabowskia Schltdl. are included in our data as Lycium. Also, following Levin and Miller [20], Lycium prunus-spinosa is considered to be Lycium cinereum and Lycium sandwicense is now Lycium carolinianum. The details of the species names and GenBank accession numbers for all DNA sequences are available in supplementary (Tables S1 and S2). In addition, the following species were included as outgroups [7,9,33]: Nolana albescens, Nolana rostrata, Nolana sp. A, Nolana sp. B, Sclerophylax sp., Jaborosa_integrifolia, and Jaborosa squarrosa.
Based on the combined DNA dataset (all six markers), we used BEAUti v.1.8.3 [34] to reconstruct a dated complete phylogenetic tree employing the Bayesian Markov chain Monte Carlo (MCMC) approach implemented in the program BEAST v.1.8.3 [34]. The model GTR+I+Γ (i.e., with a significant proportion of invariable sites and a gamma distribution accounting for rate variation among sites) was selected in the process of dated tree reconstruction based on Akaike Information Criterion (AIC) [35] evaluated using MODELTEST [36]. In addition, the birth–death prior with uncorrelated relaxed lognormal model for rate variation among branches was selected. To calibrate the Lycium tree, we used the normal priors with age estimates from data of a wide range of angiosperms (2.4–2.6 × 10−10 substitutions, Bousquest et al. [37]). Markov chain Monte Carlo (MCMC) was run for 15 million generations, and trees were sampled every 10,000 generations. The resulting log files, including the prior and likelihood values as well as effective sample size (ESS), were analyzed using Tracer 1.5 [38]. The ESS values ranged from 300 to 800 for the age estimates, suggesting that they were reliable age estimates. The first 25 (i.e., 2500) of the resulting 10,000 trees were discarded as burn-in using TreeAnnotator v 1.6.1 [39] to generate the maximum clade credibility (MCC) tree. The node support on the BEAST tree was interpreted as not supported when PP < 0.50 and well supported when PP > 0.90.

2.2. Ancestral Area Reconstruction States: Historical Biogeography of Lycium

Prior to analysis, species were grouped according to their current geography: (A) Eurasia, (B) Australia, (C) South Africa, (D) North America, (E) Pacific Island, and (F) South America. Then, fitting the Bayesian Binary Model (BBM), as implemented in RASP, we reconstructed the likely ancestral ranges along the phylogeny of Lycium. In the process of ancestral area reconstructions, at a node on the phylogeny, all of the frequencies of an ancestral range generated for all RASP-generated trees in Bayesian analysis were averaged [40]. Specifically, we simultaneously ran MCMC chains over 5,000,000 generations and we used 20,000 trees from the MCMC output generated with BBM. Every 1000 generations, the state was sampled, and we used fixed JC + G (Jukes-Cantor + Gamma) with null root distribution. The maximum number of possible areas was kept as 3.

2.3. Diversification Analysis

Our diversification analyses were run in R library TESS [41]. Firstly, we calculated the net diversification rate using the R function bd.ms. Then, using the R function ‘branching.times’, we calculated the frequency distribution of the speciation events within the genus to determine when most of the branching events (speciation events) occurred. Finally, we investigated if the speciation and overall diversification rate departed significantly from the null expectation (constant-rate birth–death model). To this end, we calculated the observed gamma value for the genus and compared this value to that of the posterior-predictive distribution of 1000 simulated trees under a constant-rate birth–death model. The 95% Credible Interval (CI) of the posterior-predictive distributions was then determined to assess if the observed gamma is different from the expectation.

2.4. Quantifying the Evolutionary Events That Shaped the Diversification of the Genus Lycium

To determine the evolutionary events that have shaped the diversification within the genus, we performed a Compound Poisson Process on Mass Extinction Time (CoMET), as implemented in the R library TESS [41]. In this analysis, the number of speciation-rate shifts, extinction rate shifts, and mass-extinction events were treated as random variables, and their joint posterior distributions were estimated. The advantage of this approach is that it allows not only all possible birth-death models to be fitted, but also for mass extinction to be modeled.

3. Results

3.1. Phylogeny

We distinguish three clades on the phylogeny (A–C, Figure 1 and Figure S1). The clade “A”, well supported (PP = 1.00), is mainly composed of southern African species. However, within clade A are embedded Chinese, European, and Australian species, suggesting that Eurasian and Australian species may have originated from southern Africa. This topology also implies that clade A (southern Africa + Eurasia + Australia) is monophyletic. Then, we have clade “B”, moderately supported (PP = 0.7, Figure 1) and made up of species from South and North America. A South American species (L. bridgesii) is sister (PP = 0.7) to clade B. Another South American species, L. boerhaviifolia, is sister (PP = 1.00) to the remainder of the clade, which is of North American origin. In the last clade (clade C), with high support (PP = 1.0), South American and then North American species alternate along the phylogeny. It is also noteworthy to mention that Pacific Island species are embedded in clade C.

3.2. Reconstruction of Historical Biogeography

Our analysis points to South America as the origin of the genus (100%). Then, through dispersals, North America may have been colonized around 15 mya. Through mostly dispersal events, first southern Africa witnessed the diversification of the genus, and from southern Africa, Eurasian and Australian species radiated and diversified (Figure 2).

3.3. Diversification Analysis

The frequency distribution of the branching times shows that most of speciation events took place in the last 5 million years (Figure 3a). Our estimate of the net diversification r = 0. 0.1441. We also found evidence of an increasing species accumulation through time until the present day (Ɣ = 0.60, CI = [−1.35:2.73], Figure 3b). However, the overall pattern of this diversification does not depart significantly from random expectation (Figure 3b), suggesting an overall constant-rate diversification of the genus Lycium.
This overall constant-rate diversification is evidenced in the outcomes of the analysis of the Compound Poisson Process (CPP) on mass extinction time (Figure 4). Indeed, the speciation rate remains roughly constant at r = 0.2 throughout the diversification period of the genus (Figure 4a). Also, ten significant speciation shifts are observed (Figure 4b). Furthermore, the extinction rate remains overall roughly constant around r~0.05 and throughout the diversification period (Figure 4c), although 11 significant extinction shifts occurred (Figure 4d) with one significant mass extinction around 23 mya (Figure 4e,f).

4. Discussion

4.1. Phylogeny

Topologically, our phylogeny is similar to what was reported in other studies. Specifically, the New and Old World’s species do not have the same origin on the phylogeny (paraphyly) and the largely southern African clade (our clade A), which harbors Australian and Eurasian species (monophyly, [7,8,9,33]). Also, our phylogeny supports the unreliability of several morphological features [42] used to delimit sections within the genus. For example, the feature ‘unicarpellate ovary’, considered apomorphic, is relied upon to delimit the section Sclerocarpellum [4,14], which includes only two species (L. ameghinoi and L. californicum). L. cestroides was reported to be sister to all American Lycium with moderate support [33]. In the present study, however, L. cestroides appears sister (PP = 0.9) to the South American pair (L. cuneatum + L. moringii). Interestingly, as opposed to the Sections Sclerocarpellum and Lycium, which have been phylogenetically unsupported in several studies [7,8,9,42], the Section Schistocalyx, with its two species Lycium chilense and L. ciliatum, is monophyletic and well supported in the present study (PP = 1.00). They both share morphological features, including an enlarged ciliate base on the filaments [13,14], prompting some authors to wonder whether they should not be lumped together as one species [7]. Lycium chilense is found in Argentina and Chile [13] and at >3470m asl in the Andes, whilst L. ciliatum’s ranges spread from Argentina to Bolivia [13]. Finally, the Australian species L. australe is embedded within our clade A, which is a predominantly southern African species. This finding matches what was previously reported [9,33], suggesting that the Australian species may have its origin in southern Africa. Overall, our phylogeny recovers key clades reported in other studies, but with more reliable node supports in some instances.

4.2. Biogeography Analysis

The biogeography of the genus Lycium is well investigated (e.g., [7,20,21]). In their study, Fukuda et al. [7] indicated that the genus Lycium originated from the New World around 29.4 ± 9.7 mya, but their analysis failed to determine whether the genus is of South or North American origin. Miller et al. [21] confirmed the America’s origin and suggested that the genus may have initially dispersed from the Americas to Africa around and then to Asia. In our study, we specifically show with high probability that Lycium originated from South America. In addition, at the origin, we found no evidence of vicariance but, rather, dispersal events, supporting earlier studies [20,21]. Specifically, we demonstrated that the genus, from South America, first colonized southern Africa, and from southern Africa later reached Eurasia and Australia, and all of these colonization events occurred mainly through long-distance dispersals. Our analysis, therefore, disproves once again the vicariance hypothesis, which attributes the disjunct geography of the genus to the drifting of landmasses following the breakup of the Gondwana [18]. Our finding is further supported by the timing of the breakup event in comparison to the timing of the diversification of the genus. Indeed, our dated phylogeny with six DNA markers places the origin of the genus in South America around 25 mya (29.4 ± 9.7 mya in Fukuda et al. [7]) whereas the breakup of the continental masses occurred earlier in the Cretaceous to pre-Cenozoic period around 60–80 mya (e.g., [42]). Since our analysis points toward a higher probability of the predominance of dispersal events underlying the observed distribution of the genus (see also Cao et al. [10]), the present study therefore provides an additional support to the dispersal hypothesis championed in an early study [19]. However, it is important to highlight a few signatures of recent vicariance events, specifically between Lycium americanum Jacq., which grows primarily in the seasonally dry tropical habitats, and L. infaustum Miers, which grows primarily in the temperate habitats, suggesting that habitat climatic differences may be the barrier promoting potential vicariances between those species.
Then, the question becomes how the predominant long dispersal events may have taken place. Oceanic dispersal is increasingly referred to as the main force creating this disjunct geographic pattern (e.g., [20,43]). Our first hypothesis is that the dispersal events are bird-mediated, and this dispersal mode may have been favored by the small size and light weight of Lycium’s seeds; their seed length ranged from 1.90 to 3.06 mm and width from 1.43 to 2.53 mm, whereas their seed weight varied from 0.54 to 3.54 mg [44]. These small-sized seeds are easily carried by birds over long distances [1,4,5]), and it has been shown that viable seeds could be carried in the gizzard or intestinal tract of some migratory birds for up to 8–13 days, which is long enough for a bird to ensure a long-distance dispersal [45,46]) from South America first to southern Africa and then to North America and later from southern Africa to Eurasia. Our second hypothesis is that the dispersal events can also be human-mediated. For example, we know that some South African species, e.g., Lycium ferocissimum, a spine-covered shrub, was human-introduced to Australia in the mid-1800s as a hedge plant [47]. Also, our analysis shows that most of Lycium species diverged in the last 5 million years, whereas the human lineage family Hominidae occurred 3.5 million years ago, making it possible that humans may have been a key dispersal agent across the current geography of the genus Lycium.
The species Lycium carolinianum is distributed across the Pacific Islands on Easter Island, the Ogasawara Islands, the Hawaiian Islands, and the Daitou Islands [4,48]. Our findings reveal that the group Lycium carolinianum is sister to (Lycium brevipes and L. tenuispinosum), which are both of South American origin, suggesting that the Pacific Island species L. carolinianum may have its origin in South America. However, Levin and Miller [20] clearly identified North America as the origin of L. carolinianum in the Pacific Islands because L. carolinianum is also found in North America. In the present study, L. carolinianum var. quadrifidum is the accession of the North American population and the accession is monophyletic with that of L. carolinianum var sandwicense (=L. sandwicense = L. carolinianum in the Pacific Islands).
We know that the majority of flowering plants across the Pacific islands are bird-dispersed [18]; 80% of seed plants dispersed onto the Hawaiian Islands and Easter Island are bird-mediated [49], and so too are 70% of seed plants dispersed onto the Ogasawara islands [50]. We therefore suggest that L. carolinianum may have been bird-dispersed from South America to the Pacific Islands [51,52,53].

4.3. Diversification Dynamics

Our analysis reveals that all these species diversify following a net diversification rate = 0.1441 sp. Myr−1. This places the genus among the slowest diversification rates in the plant kingdom, since the rate is at least 2 to 4 times lower than the slowest rates reported for several genera. It is even far lower than the rate reported for the angiosperms in general (1.713 sp. Myr−1) and for gymnosperms (0.721 sp. Myr−1; [54]). The net diversification rate for the genus Lycium is, however, comparable to the mean rate found for all gymnosperms (0.166 sp. Myr−1; [54]), which are well-known for their slow diversification rate (e.g., Encephalartos under high extinction rates (0.208 sp. Myr−1; [55,56]). The diversification rate of the genus Lycium is incomparable with other angiosperm genera, which experienced unparalleled radiation, e.g., the genus Dianthus (1.80–6.09 sp. Myr−1; [57]). The lower diversification rate of the genus Lycium may arise through a high background extinction rate or lower speciation rate [58,59,60].
The frequency distribution of the branching times shows that most of speciation events took place recently in the last 5 million years, suggesting that species accumulation may still be ongoing within the genus. Indeed, our analysis based on gamma statistic suggests a gradual increase in species accumulation through time until the present day, through an overall constant-rate diversification of the genus Lycium. Such gradual expansion can only arise as a result of constant speciation and extinction rates [32]. We found a roughly constant speciation and extinction rates for the genus, thus supporting the graduation expansion model of diversification within the genus Lycium. Although we observed significant multiple speciation shifts, the effects of these shifts on the overall diversification may have been offset by multiple significant extinction shifts that occurred, thus leading to an overall constant diversification. Several authors also reported a gradual increase in the model in their studies of various clades, including birds (e.g., [61]), amphibians (e.g., [62]), and plants (e.g., [63]) in the Neotropics, and this model is promoted by stable environmental conditions over time [64,65].
In conclusion, the genus Lycium did not experience an unusually high diversification rate. Rather, it underwent multiple speciation and extinction events and even mass extinction events, which resulted in an overall constant-rate diversification of the genus Lycium.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16110680/s1, Table S1. GenBank accession numbers; Table S2. Summary of DNA matrix; Figure S1. Phylogenetic tree showing node bars.

Author Contributions

Conceptualization, H.C. and K.Y.; methodology, H.C., L.M. and K.Y.; software, K.Y. and L.M; validation, K.Y.; formal analysis, H.C., L.M. and K.Y.; investigation, H.C., L.M. and K.Y.; resources, H.C., L.M. and K.Y.; data curation, L.M.; writing—original draft preparation, K.Y.; writing—review and editing, H.C., K.Y., X.Z., S.L. and L.M.; visualization, K.Y.; supervision, K.Y.; project administration, H.C. and K.Y.; funding acquisition, H.C. All authors have read and agreed to the published version of the manuscript.

Funding

This project was funded by the first batch of foreign intelligence introduction projects in Ningxia Province in 2023 to Chen Haikui, Key construction funds of the school of biological science and engineering is acknowledged.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The phylogeny analyzed in this study is available as Supplemental Information in this manuscript.

Acknowledgments

The first batch of foreign intelligence introduction projects in Ningxia Province in 2023 to Chen Haikui, Key construction funds of the school of biological science and engineering is acknowledged. We also thank all of the reviewers who contributed to an improved manuscript.

Conflicts of Interest

The author declares no conflicts of interest. The funder had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 1. A dated phylogenetic tree of the genus Lycium from combined six genes based on Bayesian inference. The numbers above the branches represent a Bayesian posterior probability greater than 0.5 (PP > 0.5), and the branches without PP values were PP < 0.5.
Figure 1. A dated phylogenetic tree of the genus Lycium from combined six genes based on Bayesian inference. The numbers above the branches represent a Bayesian posterior probability greater than 0.5 (PP > 0.5), and the branches without PP values were PP < 0.5.
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Figure 2. A graphical output from RASP showing the results of the ancestral reconstruction area from the BBM (Bayesian Binary Method) analysis. Pie charts at each node show the probabilities of alternative ancestral ranges. The green circles around the node represent vicariance events, and the blue circles represent dispersal events. The probability of the origin at these nodes are also indicated (%).
Figure 2. A graphical output from RASP showing the results of the ancestral reconstruction area from the BBM (Bayesian Binary Method) analysis. Pie charts at each node show the probabilities of alternative ancestral ranges. The green circles around the node represent vicariance events, and the blue circles represent dispersal events. The probability of the origin at these nodes are also indicated (%).
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Figure 3. Patterns of speciation within the genus Lycium. (a) Frequency of speciation events showing that the highest frequency of speciation occurred within the last five years (red) and the remaining speciation events in the last 20 years (gray); (b) actual gamma value (x) in comparison to simulated gamma values under a model of constant diversification.
Figure 3. Patterns of speciation within the genus Lycium. (a) Frequency of speciation events showing that the highest frequency of speciation occurred within the last five years (red) and the remaining speciation events in the last 20 years (gray); (b) actual gamma value (x) in comparison to simulated gamma values under a model of constant diversification.
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Figure 4. Summary of all evolutionary events reported in this study by fitting the CoMET model. Results reported are for the diversification hyperpriors specified a priori. (a) Speciation rate; (b) speciation shift times; (c) extinction rates; (d) extinction shift times; (e) mass extinction Bayes factors; (f) mass extinction times.
Figure 4. Summary of all evolutionary events reported in this study by fitting the CoMET model. Results reported are for the diversification hyperpriors specified a priori. (a) Speciation rate; (b) speciation shift times; (c) extinction rates; (d) extinction shift times; (e) mass extinction Bayes factors; (f) mass extinction times.
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MDPI and ACS Style

Chen, H.; Yessoufou, K.; Zhang, X.; Lin, S.; Mankga, L. Multiple Speciation and Extinction Rate Shifts Shaped the Macro-Evolutionary History of the Genus Lycium Towards a Rather Gradual Accumulation of Species Within the Genus. Diversity 2024, 16, 680. https://doi.org/10.3390/d16110680

AMA Style

Chen H, Yessoufou K, Zhang X, Lin S, Mankga L. Multiple Speciation and Extinction Rate Shifts Shaped the Macro-Evolutionary History of the Genus Lycium Towards a Rather Gradual Accumulation of Species Within the Genus. Diversity. 2024; 16(11):680. https://doi.org/10.3390/d16110680

Chicago/Turabian Style

Chen, Haikui, Kowiyou Yessoufou, Xiu Zhang, Shouhe Lin, and Ledile Mankga. 2024. "Multiple Speciation and Extinction Rate Shifts Shaped the Macro-Evolutionary History of the Genus Lycium Towards a Rather Gradual Accumulation of Species Within the Genus" Diversity 16, no. 11: 680. https://doi.org/10.3390/d16110680

APA Style

Chen, H., Yessoufou, K., Zhang, X., Lin, S., & Mankga, L. (2024). Multiple Speciation and Extinction Rate Shifts Shaped the Macro-Evolutionary History of the Genus Lycium Towards a Rather Gradual Accumulation of Species Within the Genus. Diversity, 16(11), 680. https://doi.org/10.3390/d16110680

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