Gonadal Dysfunction in Abnormal-Looking Anoles Is Consistent with Hybridization and Reproductive Isolation
Species-level diversification (speciation) results from the evolution of reproductive isolation. When reproductive isolation is intrinsic (independent of ecological context), speciation is thought to be irreversible. Intrinsic reproductive isolation manifests as a reduction in hybrid fitness due to Dobzhansky-Muller incompatibilities, and can render hybrids sterile or inviable. During fieldwork in western Cuba, I identified abnormal-looking individuals with small gonads within an assemblage of Anolis. I hypothesized that such individuals were interspecific hybrids and predicted a phenotypic distinctness and lower reproductive fitness. I evaluated my predictions by comparing putative hybrids with candidate parental species in external phenotypic traits and gonadal indicators of reproductive fitness. I found that putative hybrids were phenotypically distinct and did not produce sperm cells, suggesting that hybrid sterility may be important in maintaining species boundaries in this ecologically complex system.
Dewlaps of four candidate parental species of Anolis and their putative hybrids from Sierra de Canalete, Pinar del Río, Cuba.
Map of the Guaniguanico mountain range showing the location of the study site at Sierra de Canalete (white star).
Typical mogote formation (top; photo copyright Richard Glor) and characteristics of the hole microhabitat inside the mogote where putative hybrids were found (bottom; photo by Javier Torres).
Linear discriminant analysis of four candidate parental species of Anolis lizards and their putative hybrids from Sierra de Canalete, Pinar del Río, Cuba. LD1 vs. LD2 discriminates between all categories but Anolis mestrei and putative hybrids (left panel), which are resolved in LD3 vs. LD4 (right panel) except for one individual (01R248, pointed with arrow). Overall, all categories (each species and putative hybrids) are distinct (Wilks’ k = 0.0003, F4,29 = 6.819, P < 0.001).
Variation in testes diameter (top panel) and seminiferous tubules (ST, bottom panel) among candidate parental species of Anolis and their putative hybrids from Sierra de Canalete, Pinar del Río, Cuba. Differences among classes are significant for testes diameter (F29 = 41.92, P < 0.001) and seminiferous tubules (F29 = 22.05, P < 0.001). In the putative hybrid, both gonads are delimited by a white contour. Dot = mean, box = standard error, whiskers = standard deviation. Statistical differences are indicated by different letters.
Percentage of cell types in the germinal epithelium of candidate parental species of Anolis and their putative hybrids from Sierra de Canalete, Pinar del Río, Cuba. Black = spermatogonia, dark gray = primary spermatocyte, medium gray = secondary spermatocyte, light gray = spermatids + sperm cells.
Cross-sections of testicles of Anolis from Sierra de Canalete, Pinar del Río, Cuba: (A) adult Anolis allogus, (B) adult-sized putative hybrid, and (C, D) subadult-sized A. porcatus. (1) Spermatogonium, (2) primary spermatocyte, (3) secondary spermatocyte, (4) sperm cells, (5) lumen of the seminiferous tubule with secretions, and (6) interstitial cells; asterisk marks secretions within the seminiferous tubule. Note differences in putative hybrids including disorganization of structures, much smaller size of seminiferous tubules, lower secretion activity, and lower cell production, especially of sperm cells. Magnification is 400x (A–C) and 40x (D). (Photos C, D copyright Ana Sanz.)
Variation in the number of spermatids and spermatozoa in the seminiferous tubules (top, F29 = 36.77, P < 0.001) and in the epididymis (bottom, F29 = 9.83, P < 0.001) of the candidate parental species of Anolis and their putative hybrids from Sierra de Canalete, Pinar del Río, Cuba. Dot = mean, box = standard error, whiskers = standard deviation. Statistical differences are indicated by different letters. Note differences, including lower production and storage of sperm cells in putative hybrids. Taxa selection was based on image quality but all had the same condition.
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