Species Delimitation and Conservation in Taxonomically Challenging Lineages: The Case of Two Clades of Capurodendron (Sapotaceae) in Madagascar
<p>PCA scatter plot of the first two dimensions based on 22 morphological characters and 123 specimens. Black dots within the <span class="html-italic">Capurodendron mandrarense</span> cluster represent putative hybrids between that species and <span class="html-italic">C. androyense</span> (specimens 150 and 161 in <a href="#plants-10-01702-t001" class="html-table">Table 1</a>).</p> "> Figure 2
<p>Proportion of heterozygous sites for exons (average 0.051, sd 0.013) and microsatellite flanking regions (0.045, sd 0.014), with average and standard deviation of each taxa indicated.</p> "> Figure 3
<p>Pseudocoalescent ultrametric phylogenetic tree from Astral inferred from RAxML analyses of (<b>A</b>) 600 gene exonic regions, (<b>B</b>) 608 gene supercontigs including introns, exons and flanking regions and (<b>C</b>) 195 microsatellite flanking regions. All specimens contained less than 20% missing nucleotide positions. Colors refer to morphospecies. Pie charts represent the proportion of gene trees that support the clade of interest (red), support the main alternative bifurcation (blue), or support any other remaining alternative solution (gray). Astral posterior probabilities higher than 0.8 are depicted only for interspecific clades as bold lines. Species names are followed by the specimen number used in this study and the collector code.</p> "> Figure 4
<p>Split network computed from uncorrected P-distances and a concatenated supermatrix of exonic regions from 600 genes and 81 specimens. Splits and picture margin are color-coded according to morphospecies and specimens detected as hybrids are indicated. Numbers refer to specimens in <a href="#plants-10-01702-t002" class="html-table">Table 2</a>. (Outgroups: <span class="html-italic">Bemangidia lowry</span>, <span class="html-italic">Capurodendron delphinense</span> and <span class="html-italic">C. birkinshawii</span>).</p> "> Figure 5
<p>Principal Components Analysis (PCA) of 227 microsatellite flanking regions of (<b>A</b>) the complete dataset, (<b>B</b>) the Arid Species Complex, and (<b>C</b>) the Western Species Complex. The distribution map of the samples of the Arid Complex is shown on the righ side. Specimens 120 and 41 here included under <span class="html-italic">Capurodendron microphyllum</span>, share some morphological characters with <span class="html-italic">C. androyense</span>.</p> "> Figure 6
<p>Potential distribution maps predicted by Maxent for <span class="html-italic">Capurodendron androyense</span>, <span class="html-italic">C. greveanum</span>, <span class="html-italic">C. greveanum-mandrarense</span>, <span class="html-italic">C. mandrarense</span>, <span class="html-italic">C. microphyllum</span>, <span class="html-italic">C. oblongifolium</span>, <span class="html-italic">C. perrieri</span> and <span class="html-italic">C. pervillei</span>.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
- i.
- An ongoing sympatric speciation: Although the morphospecies have a widely overlapping distribution, they show different environmental preferences (Figure 6). Capurodendron androyense is the more drought-resistant taxon, extending to the areas with 12 ecologically dry months found along the coast in the extreme south, while C. mandrarense prefers relatively more humid habitats, is more cold-tolerant, and has a distribution extending to south-central regions up to 1000 m elevation. Hence, a partially ongoing sympatric speciation mediated by environmental selection might be at work. In such a case, the area with the highest nucleotide diversity, which coincides with the genetic clusters Capurodendron androyense 2 and C. mandrarense 2 (Table 5; Figure 5) representing the majority of the complex distribution area, could correspond to the diversification center. This is a climatically intermediate area with two less months of dry season than the coastal region, while also escaping the colder night temperatures of the central highlands. From this region, the ancestral species could have undergone a selection pressure towards aridity (enforcing the Capurodendron androyense gene pool), and towards more humid and colder habitats (enforcing the C. mandrarense gene pool). Then, Capurodendron androyense 1 and C. mandrarense 1 of Figure 5 would have appeared later, having many fewer introgression signals between them and being therefore genetically ‘purer’. This pattern would correspond to a parapatric speciation process driven by ecological adaptation. In such a scenario of recent speciation, it is not surprising to observe such levels of incomplete lineage sorting (ILS), as the two species are additionally found in large areas and are expected to have high population effective sizes [67].
- ii.
- A past allopatric speciation followed by secondary contact: Under this hypothesis the species would have originated in allopatry from a recent common ancestor, adapting to different environments. Posteriorly, Capurodendron androyense and C. mandrarense distributions would have expanded and come into contact, producing the more admixed C. androyense group 2 and C. mandrarense group 2. In this scenario, the higher nucleotide diversity of these groups would point to a secondary contact with introgression rather than to an ancient center of diversification. This would parallel a similar situation to the east, where hybrids between Capurodendron androyense and C. microphyllum (a genetically well differentiated species, sister to the Arid Complex) appear in areas where both taxa coexist. In this case, ILS signal would come from admixture.
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Morphospecies | Details | |
---|---|---|
Western Complex | C. oblongifolium | Well delimited, >50 km inland, sympatric with C. pervillei. |
C. perrieri | Well delimited, <50 km from the coast, sympatric with C. pervillei. | |
C. pervillei | Well delimited, widespread and sympatric with both C. oblongifolium and C. perrieri. | |
C. aff. pervillei | Similar to C. pervillei, not monophyletic, rare occurrences scattered in the global area of the complex. | |
Arid Complex | C. androyense | Widespread, well delimited morphologically, except three specimens intermediate with C. microphyllum and two with C. mandrarense. |
C. greveanum-mandrarense | Restricted range N of Toliara, weakly delimited morphologically, characters shared with C. greveanum and C. mandrarense. | |
C. mandrarense | Widespread, variable, weakly differentiated from C. greveanum-mandrarense but more hairy and with prominent nerves. Two specimens intermediate with C. androyense. | |
Similar species | C. greveanum | Widespread in two disjunct coastal populations. Weakly differentiated from C. greveanum-mandrarense, but completely glabrous vegetatively. Phylogenetically far from the Arid Complex. |
C. microphyllum | Restricted range W of Fort-Dauphin, well delimited except three specimens intermediate with C. androyense. Sister species to the Arid Complex. |
Lab. Code | Morphospecies | Region | Collector Code | Year | Origin 1 |
---|---|---|---|---|---|
128 | Capurodendron androyense | Atsimo-Andrefana | Gautier 6328 | 2017 | Silica gel (G) |
141 | C. androyense | Atsimo-Andrefana | Gautier 6343 | 2017 | Silica gel (G) |
139 | C. androyense | Atsimo-Andrefana | Gautier 6346 | 2017 | Silica gel (G) |
140 | C. androyense | Atsimo-Andrefana | Gautier 6358 | 2017 | Silica gel (G) |
138 | C. androyense | Atsimo-Andrefana | Gautier 6361 | 2017 | Silica gel (G) |
143 | C. androyense | Androy | Gautier 6370 | 2017 | Silica gel (G) |
144 | C. androyense | Androy | Gautier 6371 | 2017 | Silica gel (G) |
125 | C. androyense | Androy | Gautier 6372 | 2017 | Silica gel (G) |
145 | C. androyense | Androy | Gautier 6374 | 2017 | Silica gel (G) |
126 | C. androyense | Androy | Gautier 6376 | 2017 | Silica gel (G) |
127 | C. androyense | Anosy | Gautier 6387 | 2017 | Silica gel (G) |
149 | C. androyense | Anosy | Randrianaivo 2954 | 2017 | Silica gel (G) |
29 | C. androyense | Anosy | Randrianaivo 2959 | 2017 | Silica gel (G) |
79 | C. androyense | Atsimo-Andrefana | Rogers 474 | 2004 | G |
70 | C. androyense | Atsimo-Andrefana | Rakotomalaza 1719 | 1998 | G |
150 | C. androyense-mandrarense | Atsimo-Andrefana | SF 22230 | 1962 | G |
161 | C. androyense-mandrarense | Atsimo-Andrefana | SF 22286 | 1962 | G |
56 | C. birkinshawii | Anosy | Birkinshaw 438 | 1997 | G |
98 | C. delphinense | Anosy | Gautier 5801 | 2011 | Silica gel (G) |
151 | C. gracilifolium | Melaky | Gautier 5736 | 2011 | Silica gel (G) |
8 | C. gracilifolium | Atsimo-Andrefana | Gautier 6318 | 2017 | Silica gel (G) |
182 | C. gracilifolium | Menabe | Randrianaivo 2972 | 2017 | Silica gel (G) |
156 | C. gracilifolium | Atsimo-Andrefana | Messmer 607 | 1998 | G |
9 | C. greveanum | DIANA | Randriarisoa 28 | 2017 | Silica gel (G) |
11 | C. greveanum | Atsimo-Andrefana | Ranaivojaona 267 | 2000 | G |
10 | C. greveanum | Menabe | Randrianaivo 2974 | 2017 | Silica gel (G) |
163 | C. mandrarense | Anosy | Andriamihajarivo 1532 | 2004 | G |
20 | C. mandrarense | Atsimo-Andrefana | Gautier 6349 | 2017 | Silica gel (G) |
21 | C. mandrarense | Atsimo-Andrefana | Gautier 6350 | 2017 | Silica gel (G) |
22 | C. mandrarense | Atsimo-Andrefana | Gautier 6351 | 2017 | Silica gel (G) |
23 | C. mandrarense | Atsimo-Andrefana | Gautier 6356 | 2017 | Silica gel (G) |
24 | C. mandrarense | Androy | Gautier 6366 | 2017 | Silica gel (G) |
25 | C. mandrarense | Androy | Gautier 6378 | 2017 | Silica gel (G) |
26 | C. mandrarense | Androy | Gautier 6379 | 2017 | Silica gel (G) |
158 | C. mandrarense | Anosy | Randrianasolo 204 | 1991 | G |
13 | C. mandrarense | Anosy | Ratovoson 1473 | 2008 | P |
159 | C. mandrarense | Anosy | Randrianaivo 1764 | 2009 | G |
110 | C. mandrarense | Anosy | Randrianaivo 1785 | 2011 | G |
27 | C. mandrarense | Anosy | Randrianaivo 2956 | 2017 | Silica gel (G) |
30 | C. mandrarense | Anosy | Randrianaivo 2960 | 2017 | Silica gel (G) |
31 | C. mandrarense | Anosy | Randrianaivo 2961 | 2017 | Silica gel (G) |
32 | C. mandrarense | Anosy | Randrianaivo 2962 | 2017 | Silica gel (G) |
33 | C. mandrarense | Anosy | Randrianaivo 2964 | 2017 | Silica gel (G) |
34 | C. mandrarense | Ihorombe | Randrianaivo 2966 | 2017 | Silica gel (G) |
35 | C. mandrarense | Ihorombe | Randrianaivo 2967 | 2017 | Silica gel (G) |
37 | C. mandrarense | Menabe | Randrianaivo 2970 | 2017 | Silica gel (G) |
38 | C. mandrarense | Menabe | Randrianaivo 2980 | 2017 | Silica gel (G) |
39 | C. mandrarense | Menabe | Randrianaivo 2981 | 2017 | Silica gel (G) |
162 | C. mandrarense | Ihorombe | SF 6692 | 1952 | G |
183 | C. mandrarense-greveanum | Atsimo-Andrefana | Andrianjafy 1679 | 2006 | P |
15 | C. mandrarense-greveanum | Atsimo-Andrefana | Gautier 6332 | 2017 | G |
16 | C. mandrarense-greveanum | Atsimo-Andrefana | Gautier 6336 | 2017 | G |
17 | C. mandrarense-greveanum | Atsimo-Andrefana | Gautier 6337 | 2017 | G |
18 | C. mandrarense-greveanum | Atsimo-Andrefana | Gautier 6339 | 2017 | G |
19 | C. mandrarense-greveanum | Atsimo-Andrefana | Gautier 6341 | 2017 | G |
160 | C. mandrarense-greveanum | Atsimo-Andrefana | McPherson 17358 | 1998 | G |
77 | C. mandrarense-greveanum | Atsimo-Andrefana | Phillipson 5603 | 2002 | G |
12 | C. mandrarense-greveanum | Atsimo-Andrefana | Razafindraibe 165 | 2006 | G |
113 | C. mandrarense-greveanum | Atsimo-Andrefana | Randrianaivo 1187 | 2005 | G |
40 | C. microphyllum | Anosy | Gautier 6382 | 2017 | Silica gel (G) |
186 | C. microphyllum | Anosy | SF 22411 | 1963 | G |
120 | C. microphyllum-androyense | Anosy | Gautier 5794 | 2011 | Silica gel (G) |
41 | C. microphyllum-androyense | Anosy | Gautier 6393 | 2017 | Silica gel (G) |
81 | C. nanophyllum (Type) | Androy | SF 28521 | 1968 | G |
46 | C. perrieri | Menabe | Noyes 1044 | 1992 | G |
47 | C. perrieri | Atsimo-Andrefana | Razakamalala 5177 | 2010 | G |
114 | C. perrieri | Boeny | Randrianaivo 969 | 2003 | G |
36 | C. perrieri | Menabe | Randrianaivo 2968 | 2017 | Silica gel (G) |
45 | C. perrieri | Menabe | Randrianaivo 2976 | 2017 | Silica gel (G) |
190 | C. oblongifolium | Boeny | PerrierBâthie 1105 | 1974 | P |
44 | C. oblongifolium | Sofia | Rakotonasolo 1601 | 2015 | G |
48 | C. oblongifolium | Sofia | Ramananjanahary 51 | 2004 | G |
49 | C. oblongifolium | Sofia | Razakamalala 1809 | 2004 | G |
76 | C. pervillei | Boeny | Labat 3557 | 2005 | G |
164 | C. pervillei | Sofia | Ramananjanahary 244 | 2004 | G |
165 | C. pervillei | Sofia | Razakamalala 1677 | 2004 | G |
50 | C. pervillei | Sofia | Randrianaivo 2397 | 2013 | G |
191 | C. aff. pervillei | Boeny | Randrianarivelo 307 | 2005 | G |
192 | C. aff. pervillei | Boeny | Randrianaivo 953 | 2003 | G |
195 | C. rubrocostatum | Boeny | Andriamihajarivo 782 | 2005 | G |
194 | C. rubrocostatum | Atsimo-Andrefana | Chauvet 187 | 1961 | G |
100 | C. rubrocostatum | Melaky | Gautier 5936 | 2012 | Silica gel (G) |
73 | C. rubrocostatum | Melaky | Luino 21 | 2012 | G |
146 | C. sp. 20 | Boeny | Gautier 6276 | 2016 | Silica gel (G) |
74(S26) | Bemangidia lowry | Anosy | Gautier 5789 | 2011 | Silica gel (G) |
Character Number | Character | Type | Coding | State |
---|---|---|---|---|
1 | Plant height | Continuous | meters | Number of meters |
2 | Brachyblast | Discrete | 0 | Absent |
1 | Present | |||
3 | Prior year’s elongating shoots | Discrete | 0 | Green and glabrous |
1 | Brown and hairy | |||
4 | Petiole length | Continuous | mm | Number of mm |
5 | Petiole hairs | Discrete | 0 | Glabrous |
1 | With hairs | |||
2 | Tomentose | |||
6 | Leaf base symmetry | Discrete | 0 | Symmetric |
1 | Asymmetric | |||
7 | Leaf base | Discrete | 0 | Decurrent |
1 | Cuneate | |||
2 | Obtuse | |||
3 | Subcordate | |||
8 | Leaf length | Continuous | mm | Number of mm |
9 | Leaf width | Continuous | mm | Number of mm |
10 | Broadest leaf region | Discrete | 0 | 1st third |
1 | 2nd third | |||
2 | 3rd third | |||
11 | Leaf apex | Discrete | 0 | Acute |
1 | Obtuse | |||
2 | Rounded | |||
3 | Emarginated | |||
12 | Leaf upper side hairs | Discrete | 0 | Glabrous |
1 | With hairs | |||
2 | Tomentose | |||
13 | Leaf lower side hairs | Discrete | 0 | Glabrous |
1 | With hairs | |||
2 | Tomentose | |||
14 | Midrib on the lower side | Discrete | 0 | Not prominent |
1 | Prominent | |||
15 | Secondary nerves on the lower side | Discrete | 0 | Not prominent |
1 | Prominent | |||
16 | Midrib hairs on the upper side | Discrete | 0 | Glabrous |
1 | With hairs | |||
2 | Tomentose | |||
17 | Midrib hairs on the lower side | Discrete | 0 | Glabrous |
1 | With hairs | |||
2 | Tomentose | |||
18 | Pairs of secondary nerves | Continuous | Number | Number of pairs |
19 | Pedicel length of flower | Continuous | mm | Number of mm |
20 | Calyx hairs | Discrete | 0 | Adpressed |
1 | Hirsute | |||
21 | External sepal length | Continuous | mm | Number of mm |
22 | Calyx diameter | Continuous | mm | Number of mm |
Specimen 191 | Specimen 192 | |
---|---|---|
Alleles in C. oblongifolium | 192 (56.8%) | 2 (0.7%) |
Alleles in C. perrieri | 2 (0.6%) | 160 (56.7%) |
Alleles in C. pervillei | 144 (42.6%) | 120 (42.6%) |
Missing/unsupported alleles | 137 | 164 |
Monospecific loci | 101 (59.7%) | 85 (60.3%) |
Heterospecific loci | 68 (40.3%) | 56 (39.7%) |
Exons Flanking Regions FST | ||||||
---|---|---|---|---|---|---|
C. androyense | C. androyense 1 | C. androyense 2 | C. mandrarense | C. mandrarense 1 | C. mandrarense 2 | |
C. androyense 1 | ‒ | |||||
C. androyense 2 | ‒ | 0.037 ± 0.073 | ||||
C. mandrarense | 0.033 +− 0.052 | ‒ | ‒ | |||
C. mandrarense 1 | ‒ | 0.090 +− 0.117 | ‒ | ‒ | ||
C. mandrarense 2 | ‒ | ‒ | 0.024 ± 0.058 | ‒ | 0.046 ± 0.074 | |
C. greveanum-mandrarense | 0.118 ± 0.114 | 0.139 ± 0.142 | 0.095 ± 0.110 | 0.104 ± 0.111 | 0.111 ± 0.122 | 0.111 ± 0.122 |
STR Flanking Regions FST | ||||||
C. androyense | C. androyense 1 | C. androyense 2 | C. mandrarense | C. mandrarense 1 | C. mandrarense 2 | |
C. androyense 1 | ‒ | |||||
C. androyense 2 | ‒ | 0.037 ± 0.079 | ||||
C. mandrarense | 0.033 ± 0.052 | ‒ | ‒ | |||
C. mandrarense 1 | ‒ | 0.084 ± 0.117 | ‒ | ‒ | ||
C. mandrarense 2 | ‒ | ‒ | 0.025 ± 0.063 | ‒ | 0.044 ± 0.081 | |
C. greveanum-mandrarense | 0.112 ± 0.112 | 0.122 ± 0.140 | 0.094 ± 0.120 | 0.108 ± 0.113 | 0.111 ± 0.139 | 0.097 ± 0.122 |
Species | Number of Points | Most Important Variables | Jackknife of AUC |
---|---|---|---|
Capurodendron androyense | 90 | Precipitation of wettest month | 0.94 |
Precipitation of wettest quarter | 0.93 | ||
Annual precipitation | 0.92 | ||
Capurodendron greveanum | 79 | Annual precipitation | 0.94 |
Annual mean temperature | 0.92 | ||
Mean temperature of warmest quarter | 0.92 | ||
Capurodendron greveanum-mandrarense | 22 | Annual precipitation | 0.97 |
Precipitation of wettest quarter | 0.02 | ||
Precipitation of wettest month | 0.91 | ||
Capurodendron mandrarense | 60 | Max temperature of warmest Month | 0.88 |
Temperature seasonality | 0.87 | ||
Temperature annual range | 0.82 | ||
Capurodendron microphyllum | 14 | Precipitation seasonality | 0.94 |
Precipitation of wettest month | 0.94 | ||
Precipitation of wettest quarter | 0.91 | ||
Capurodendron oblongifolium | 6 | Precipitation of wettest month | 0.99 |
Precipitation of wettest quarter | 0.97 | ||
Precipitation seasonality | 0.96 | ||
Capurodendron perrieri | 45 | Precipitation seasonality | 0.96 |
Mean temperature of warmest quarter | 0.94 | ||
Mean temperature of wettest quarter | 0.94 | ||
Capurodendron pervillei | 36 | Precipitation of wettest month | 0.98 |
Precipitation of wettest quarter | 0.97 | ||
Annual mean temperature | 0.97 |
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Boluda, C.G.; Christe, C.; Randriarisoa, A.; Gautier, L.; Naciri, Y. Species Delimitation and Conservation in Taxonomically Challenging Lineages: The Case of Two Clades of Capurodendron (Sapotaceae) in Madagascar. Plants 2021, 10, 1702. https://doi.org/10.3390/plants10081702
Boluda CG, Christe C, Randriarisoa A, Gautier L, Naciri Y. Species Delimitation and Conservation in Taxonomically Challenging Lineages: The Case of Two Clades of Capurodendron (Sapotaceae) in Madagascar. Plants. 2021; 10(8):1702. https://doi.org/10.3390/plants10081702
Chicago/Turabian StyleBoluda, Carlos G., Camille Christe, Aina Randriarisoa, Laurent Gautier, and Yamama Naciri. 2021. "Species Delimitation and Conservation in Taxonomically Challenging Lineages: The Case of Two Clades of Capurodendron (Sapotaceae) in Madagascar" Plants 10, no. 8: 1702. https://doi.org/10.3390/plants10081702
APA StyleBoluda, C. G., Christe, C., Randriarisoa, A., Gautier, L., & Naciri, Y. (2021). Species Delimitation and Conservation in Taxonomically Challenging Lineages: The Case of Two Clades of Capurodendron (Sapotaceae) in Madagascar. Plants, 10(8), 1702. https://doi.org/10.3390/plants10081702