Research Article |
Corresponding author: Alfonso A. González-Díaz ( agonzalez@ecosur.mx ) Academic editor: Felipe Ottoni
© 2022 Alberto Macossay-Cortez, Rocío Rodiles-Hernández, Alfonso A. González-Díaz, C. Patricia Ornelas-García, Adrián F. González-Acosta.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Macossay-Cortez A, Rodiles-Hernández R, González-Díaz AA, Ornelas-García CP, González-Acosta AF (2022) Intraspecific morphological variation in shads, Dorosoma anale and D. petenense (Actinopterygii: Clupeiformes: Clupeidae), in the Mexican Grijalva and Usumacinta river basins. Acta Ichthyologica et Piscatoria 52(2): 149-158. https://doi.org/10.3897/aiep.52.84694
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Historical hydrological changes and the environmental characteristics of northern Middle America have promoted diversification and determined the distribution of fishes in the Grijalva and Usumacinta river basins of Mexico. In several taxa with wide distributions, cryptic diversity has been identified through molecular and morphological analyses. This study evaluated the intraspecific morphological variation of Dorosoma anale Meek, 1904 and Dorosoma petenense (Günther, 1867) along the Grijalva and Usumacinta river basins through geometric morphometric and linear biometric analyses. Little intraspecific differentiation was detected for either species. However, differences were identified between populations in the Grijalva basin and those from the upper Usumacinta River basins with respect to body height, head size, pelvic fin position, and anal fin size. The phenotypic expression of these attributes appears to be closely related to habitat type and geographic isolation. The morphological differences within D. petenense support the molecular hypothesis of two lineages existing in the Usumacinta River basin.
body shape variation, geometric morphometrics, Middle-American fish, phenotypic differentiation
The highly diverse ichthyofauna of northern Middle America has a complex biogeographic history. Frequent geological, volcanic, and climatic events from the Late Cretaceous to the Miocene and Pleistocene determined the diversification and distribution of fishes in the region (
The Grijalva–Usumacinta hydrological system provides an excellent model for understanding the effects of geological and climatic events on the evolution of fish communities in northern Middle America. This hydrological system is characterized by its diversity of fish species and large amount of endemism, which is predominantly observed in the Cichlidae and Poeciliidae families (
The lower regions of the Grijalva and Usumacinta basins share many species of the same ichthyofauna (
Although cichlids and poeciliids are the most diverse and abundant fish families within the Grijalva–Usumacinta system, other families also reflect the effects of the region’s historic events. Such is the case of the genus Dorosoma, for which genetic evidence shows that cryptic diversity exists throughout the distribution of the species Dorosoma petenense (Günther, 1867) in Middle America, which consists of several lineages (
Based on the biogeographic and molecular precedents of the ichthyofauna in northern Middle America, we proposed an analysis of the intraspecific morphological variation of the shads Dorosoma anale and D. petenense throughout the Grijalva and Usumacinta rivers in Mexico. This study used linear biometric and geometric morphometric methods. Notably, both analyses are complementary and have been widely used in ichthyology to identify intra- and interspecific morphological differences and describe patterns of variation (
A total of 262 adult specimens were analyzed, corresponding to the species Dorosoma anale (n = 136, 71 males and 65 females) and D. petenense (n = 126, 44 males, 82 females). The specimens were deposited in the Fish Collection of El Colegio de la Frontera Sur (ECOSC; Table
Sample sites location of Dorosoma anale and D. petenense in the Grijalva and Usumacinta basins: 1 = Lacantún River, 2 = Lacanjá River, 3 = San Leandro Lagoon, 4 = Miramar Lagoon, 5 = Canitzán Lagoon, 6 = Chacamax River, 7 = Nueva Esperanza Lagoon, 8 = San Pedro River, 9 = Usumacinta River, 10 = San Isidro Lagoon, 11 = Pom Lagoon, 12 = Palancares Lagoon, 13 = Vapor Lagoon, 14 = Boca Chica estuary, 15 = Malpaso dam, 16 = Chicoasén dam, 17 = Peñitas dam, 18 = Tzendales River. Black triangles indicate the dams.
Location of the sampling sites and samples sizes of Dorosoma anale and D. petenese in Grijalva and Usumacinta basins.
Site | Region | Coordinates | D. anale (n = 136) | D. petenense (n = 126) |
---|---|---|---|---|
1 Lacantun River | U | 16°32′13′′N, 090°41′52′′W | 10 | 1 |
2 Lacanja River | U | 16°24′21′′N, 090°47′54′′W | 10 | 3 |
3 San Leandro Lagoon | U | 16°15′28′′N, 090°52′31′′W | 17 | 10 |
4 Miramar Lagoon | U | 16°23′40′′N, 091°15′44′′W | — | 13 |
5 Canitzan Lagoon | M | 17°35′34′′N, 091°23′46′′W | 7 | 10 |
6 Chacamax River | M | 17°41′08′′N, 091°41′11′′W | 9 | 2 |
7 Nueva Esperanza Lagoon | M | 17°47′16′′N, 091°48′30′′W | 10 | — |
8 San Pedro River | M | 16°18′48′′N, 090°53′23′′W | — | 15 |
9 Usumacinta River | M | 17°29′34′′N, 091°26′26′′W | 8 | — |
10 San Isidro Lagoon | L | 18°24′26′′N, 092°28′09′′W | 10 | 10 |
11 Pom Lagoon | L | 18°33′33′′N, 092°13′31′′W | 10 | 10 |
12 Palancares Lagoon | L | 18°33′58′′N, 092°04′33′′W | 10 | — |
13 Vapor Lagoon | L | 18°22′42′′N, 091°49′52′′W | — | 10 |
14 Boca Chica estuary | L | 18°26′46′′N, 091°47′33′′W | — | 8 |
15 Malpaso dam | G | 17°06′38′′N, 093°29′59′′W | 32 | 12 |
16 Chicoasen dam | G | 16°53′26′′N, 093°07′00′′W | 3 | 9 |
17 Peñitas dam | G | 17°27′02′′N, 093°26′03′′W | — | 9 |
18 Tzendales River | U | 16°17′20′′N, 090°54′23′′W | — | 4 |
Procrustes distances values (above diagonal) and P-values (below diagonal) to pairwise comparison test between all sections of the Grijalva–Usumacinta rivers basin to Dorosoma anale and D. petenense.
Procrustes distances | |||||
---|---|---|---|---|---|
D. anale | Lower | Middle | Upper | Grijalva | |
Lower | — | 0.0075 | 0.0109 | 0.0142 | |
Middle | 0.4219 | — | 0.0121 | 0.0136 | |
Upper | 0.064 | 0.0083 | — | 0.0164 | |
Grijalva | 0.0012 | <0.0001 | <0.0001 | — | |
D. petenense | Lower | Middle | Upper | Grijalva | |
Lower | — | 0.0111 | 0.0272 | 0.0137 | |
Middle | 0.0295 | — | 0.0228 | 0.0139 | |
Upper | <0.0001 | <0.0001 | — | 0.0324 | |
Grijalva | 0.0004 | 0.0008 | <0.0001 | — |
Specimens were photographed from the left side of the body with a Sony DSC-HX300 digital camera (10 megapixels) using a 10 mm reference scale. To characterize the body shape, we used a configuration of 18 fixed landmarks (Fig.
Location of fixed landmarks in two species of the Dorosoma genus (image modified from
Morphometric and statistical analyses. To analyze geographic intraspecific variation, specimens were classified into four groups according to the collection site. One group consisted of specimens from the Grijalva basin, while the other three were from the upper, middle, and lower regions of the Usumacinta basin (Fig.
An analysis of geometric morphometrics was conducted using MorphoJ software, version 1.07a (
With the residual values of the multivariate regression, a principal components analysis (PCA) was performed to evaluate intraspecific variation. The first two principal components were used to explore the distribution of the specimens in the morphospace and describe variation in body shape based on the deformation grids. Later, we conducted a canonical variate analysis (CVA) to determine whether significant differences in body shape exist among the four groups. Additionally, we carried out paired comparisons based on the procrustes distances. Finally, we applied a discriminant function analysis (DFA) to perform cross-validation to determine the percentage of classification of the specimens in each group based on the Mahalanobis distances. All tests subjected the data to 10,000 permutations, when appropriate.
Additionally, based on the deformation grids, we identified the body sections for which greater variation existed. We then took linear measurements to evaluate whether they are discriminant among the four groups. Measurements were obtained by using the CoordGen8 program (IMP;
Museum catalog information. Catalogue number of the specimens used in the morphometric analysis. Dorosoma anale: ECOSC 612, 658, 1286, 1737, 3492, 4426, 6708, 6714, 10713, 10714, 11748, 11752, 12549, 12555, 12665, 12790, 13521, 13533 al 13535, 13546, 13549, 13561, 13564, 13565, 13976, 14290, 14300; D. petenense: ECOSC 7339, 8698–8707, 9882–9891, 12616, 12619, 12657, 12669, 12716, 12722, 13702, 13723, 13738, 14547, 14679, 14680.
Intraspecific variation in Dorosoma anale. In the PCA, the first two components explained 42.5% of the total variance. In the morphospace, no formation of groups was observed given the extensive overlap among specimens (Fig.
(A) Morphospace formed by PC1 (36.20%) and PC2 (18.94%) for Dorosoma anale. Squares represent the upper region, triangles represent the middle region, dots represent the lower region and stars represent the Grijalva region. Deformation grids are associated to the most negative and positive values of the PC1 and PC2. (B) discriminatory linear measures expressed in percent for D. anale. U = Upper, M = Middle, L = Lower, G = Grijalva.
Meanwhile, the CVA and paired tests revealed significant differences among groups (P < 0.05). Nevertheless, the only differences among the four groups were between the Grijalva group and the three groups of the Usumacinta basin. For the Usumacinta groups, only the middle and upper regions were significantly different (P < 0.05; Table
Percentage of Dorosoma anale and D. petenense correctly classified to their a priori groups based on the discriminant function analysis.
D. anale | n | Lower | Middle | Upper | Grijalva |
Lower | 30 | 72.2 | 56.7 | 76.7 | 83.3 |
Middle | 34 | 64.7 | 72.6 | 73.5 | 79.4 |
Upper | 37 | 70.3 | 70.3 | 77.48 | 91.9 |
Grijalva | 35 | 82.9 | 85.7 | 88.6 | 85.7 |
Total | 136 | ||||
D. petenense | n | Lower | Middle | Upper | Grijalva |
Lower | 38 | 76.31 | 68.42 | 86.84 | 73.68 |
Middle | 27 | 70.37 | 72.85 | 88.89 | 59.29 |
Upper | 31 | 77.42 | 83.87 | 84.95 | 93.55 |
Grijalva | 30 | 70 | 60 | 96.67 | 75.56 |
Total | 126 |
Based on the variation in body shape observed in the deformation grids, we selected five linear measurements to evaluate their capacity to discriminate among the groups. The selected measurements were as follows: I) anterior margin of the upper mandible to the posterior margin of the operculum (landmarks 1–17); II) posterior margin of the supraoccipital crest to the anterior insertion of the anal fin (2–9); III) anterior insertion of the dorsal fin to the anterior insertion of the pelvic fin (3–10); IV) posterior insertion of the dorsal fin to the anterior insertion of the anal fin (4–9); V) anterior insertion of the anal fin to the posterior insertion of the anal fin (8–9).
In D. anale, the statistical analyses (ANOVA, Kruskal–Wallis) and respective a posteriori tests (Tukey, Mann–Whitney) revealed that only the following three measurements could discriminate at least one of the groups (P < 0.05): I) anterior margin of the upper mandible to the posterior margin of the operculum (1–17); III) anterior insertion of the dorsal fin to the anterior insertion of the pelvic fin (3–10); IV) posterior insertion of the dorsal fin to the anterior insertion of the anal fin (4–9). The box plot of these three measurements (expressed in proportions) allowed us to determine that the groups with the greatest variation were from the upper regions of the Usumacinta and Grijalva basin (Fig.
Intraspecific variation in Dorosoma petenense. In the PCA, the first two components explained 42.73% of the total variance. In PC1 (25.19%), we observed a substantial overlap of the four groups on the negative axis. However, on the positive axis, specimens from the upper Usumacinta appeared to diverge, especially from Site 4 (Miramar Lagoon, Fig.
(A) Morphospace formed by PC1 (25.1%) and PC2 (17.5%) for Dorosoma petenense. Squares represent the upper region, triangles represent the middle region, dots represent the lower region and stars represent the Grijalva region. Deformation grids are associated to the most negative and positive values of the PC1 and PC2. (B) discriminatory linear measures for D. petenense. U = Upper, M = Middle, L = Lower, G = Grijalva.
The CVA and paired tests showed significant differences among the four groups (P < 0.05; Table
Multivariate analyses (ANOVA, Kruskal–Wallis) of the five linear measurements and the corresponding a posteriori tests showed that four measurements are discriminant (P < 0.05): II) posterior margin of the supraoccipital crest to the anterior insertion of the anal fin (2–9); III) anterior insertion of the dorsal fin to the anterior insertion of the pelvic fin (3–10); IV) posterior insertion of the dorsal fin to the anterior insertion of the anal fin (4–9); V) anterior insertion of the anal fin to the posterior insertion of the anal fin (8–9). Statistical differences were observed in the groups of the upper Usumacinta and the Grijalva. The diagrams of the four measurements (expressed in proportions) suggest that the groups that differed most were from the upper Usumacinta and the Grijalva (Fig.
Little intraspecific morphological differentiation was observed within Dorosoma anale and D. petenense throughout their distribution in the Grijalva and Usumacinta basins. Nevertheless, patterns of variation and morphological differences were identified in some of the geographic groups, which allowed us to assume that some regional historic and/or ecological processes were involved in creating and maintaining the phenotypic differentiation in both species. In the Clupeiformes and other fish taxa, migratory behavior and tolerance to salinity could have important implications for morphological differentiation (
In the morphospace of D. anale, no separation among groups by geographic location was observed. However, among specimens of the upper Usumacinta basin, variation existed in terms of head size, body depth, and fin position. This could be related to the type of habitat since the separation was observed among specimens from the river (sites 1, 2, and 18) and lake habitats (sites 3 and 4). Additionally, comparisons among geographic groups based on the statistical tests showed that the specimens of the Grijalva basin were differentiated by having shallower bodies.
A similar pattern of variation was observed in the morphospace of D. petenense, while the overlap between the four geographic groups was also found. Nevertheless, specimens of the upper Usumacinta tended to be differentiated from the rest of the groups by having a deeper body. Within the upper Usumacinta group, the separation from specimens of the Miramar Lagoon was notable (Fig.
In both species, the greatest intraspecific morphological variation was principally observed in body shape, head size, and fin position. For many diverse species of fish, it has been demonstrated that variation in these anatomic attributes has functional importance and has been correlated with environmental factors such as water current speed, habitat structure, and the presence of predators (
Nevertheless, despite morphological evidence indicating that ecological-environmental factors may be promoting phenotypic differentiation in both species between the Grijalva and upper Usumacinta groups, the effect of geographic isolation and distance should also be considered—particularly for specimens of the Grijalva, which are the most geographically isolated (
The morphological differentiation among D. petenense specimens in the upper Usumacinta appears to corroborate part of the hydrological history of the basin (
Although morphological variation in the same anatomical attributes was found in both species, D. anale is less variable than D. petenense, mainly observed in the upper Usumacinta populations. Contrary to our expectations, despite being closely related and having similar ecological requirements, the magnitude and direction of morphological changes were distinct. This has also been found for other groups of fish for which the level of morphological variation among species is related to the level of dietary specialization (
Differences in the patterns of variation found in D. anale and D. petenense once again demonstrated that the phenotypic expression of morphological characteristics is a product of the interaction among diverse biological, environmental, and historic processes (
There is little intraspecific variation in body shape in D. anale and D. petenense. However, we uncovered statistically significant differences between specimens of both species from the Grijalva basins and the upper Usumacinta. Morphological differentiation was based on body height, head length, pelvic fin position, and anal fin length. Nevertheless, even though variation was observed for the same attributes in both species, the direction and magnitude differed. Since the variation in these morphological attributes seems to be related to biological, environmental, and geographic factors, it could serve to define ecotypes. For both species, morphological differences among specimens from the Grijalva basin could be due to geographic isolation. Meanwhile, differentiation among D. petenense specimens from the upper Usumacinta appears to support the hypothesis regarding the existence of two lineages in the Usumacinta basin. Additionally, in D. petenense, differentiation was detected among specimens from the Miramar Lagoon. Notably, there is a need for further taxonomic and biogeographic studies of the ichthyofauna in northern Middle America to better comprehend their diversity and the processes related to their evolution—particularly in the Grijalva and Usumacinta basins, which possess some of the most interesting and complex fish communities of the Neotropics.
We thank the anonymous reviewers who provided helpful comments that improved the manuscript. AMC thanks to the Consejo Nacional de Ciencia y Tecnología (CONACYT) for the scholarship 297018 granted for the period of 2017–2020. Financial support for this study was received from the project “Conectividad y diversidad funcional de la Cuenca del río Usumacinta” (Fondo de investigación Científica y Desarrollo Tecnológico de El Colegio de la Frontera Sur, FID-784), coordinated by RRH. AFGA thanks to COFAA and EDI_IPN Programs, and SNI-CONACYT