Trends in evolution of the Rhodniini tribe (Hemiptera, Triatominae): experimental crosses between Psammolestes tertius Lent & Jurberg, 1965 and P. coreodes Bergroth, 1911 and analysis of the reproductive isolating mechanisms

Abstract

Background The tribe Rhodniini is a monophyletic group composed of 24 species grouped into two genera: Rhodnius and Psammolestes. The genus Psammolestes includes only three species, namely P. coreodes, P. tertius and P. arthuri. Natural hybridization events have been reported for the Rhodniini tribe (for genus Rhodnius specifically). Information obtained from hybridization studies can improve our understanding of the taxonomy and systematics of species. Here we report the results from experimental crosses performed between P. tertius and P. coreodes and from subsequent analyses of the reproductive and morphological aspects of the hybrids. Methods Crossing experiments were conducted between P. tertius and P. coreodes to evaluate the pre- and post-zygotic barriers between species of the Rhodniini tribe. We also performed cytogenetic analyses of the F1 hybrids, with a focus on the degree of pairing between the homeologous chromosomes, and morphology studies of the male gonads to evaluate the presence of gonadal dysgenesis. Lastly, we analyzed the segregation of phenotypic characteristics. Results Interspecific experimental crosses demonstrated intrageneric genomic compatibility since hybrids were produced in both directions. However, these hybrids showed a high mortality rate, suggesting a post-zygotic barrier resulting in hybrid unviability. The F1 hybrids that reached adulthood presented the dominant phenotypic segregation pattern for P. tertius in both directions. These insects were then intercrossed; the hybrids were used in the cross between P. tertius ♀ × P. coreodes ♂ died before oviposition, and the F1 hybrids of P. coreodes ♀ x P. tertius ♂ oviposited and their F2 hybrids hatched (however, all specimens died after hatching, still in first-generation nymph stage, pointing to a hybrid collapse event). Morphological analyses of male gonads from F1 hybrids showed that they did not have gonadal dysgenesis. Cytogenetic analyses of these triatomines showed that there were metaphases with 100% pairing between homeologous chromosomes and metaphases with pairing errors. Conclusion The results of this study demonstrate that Psammolestes spp. have intrageneric genomic compatibility and that post-zygotic barriers, namely unviability of hybrid and hybrid collapse, resulted in the breakdown of the hybrids of P. tertius and P. coreodes, confirming the specific status of species based on the biological concept of species. Graphical abstract

Phylogenetic relationships and evolutionary patterns of the genus Psammolestes Bergroth, 1911 (Hemiptera: Reduviidae: Triatominae)

“…This finding agrees with previous studies that documented nonoverlapping niches for P. coreodes and P. tertius [ 30 , 32 ]. Such an scenario of niche divergence agrees with the absence of gene flow between the three species and the inviability reported in experimental crosses between P. tertius and P. coreodes [ 38 ]. However, the relevance of other factors in species divergence, such as biotic interactions need to be investigated.…”

“…We recovered three well supported lineages that are concordant with the previously described morphospecies and experimental crosses: P. coreodes, P. tertius and P. arthuri [ 38 ]. Both phylogenetic and population genetics analyses indicate that P. coreodes and P. tertius are genetically more similar than they are to P. arthuri .…”

“…This result is consistent both with the geographic and genetic distance between these taxa. Despite of the contentious systematics of the genus [ 28 , 40 – 44 ], all our analyses validate the existence of three lineages of Psammolestes thus supporting the original species description based on morphological traits [ 31 , 35 , 38 ].…”

“…Specifically, P. tertius has basal plate struts broadly S-shaped, while those of P. coreodes are hook shaped. Also, the anteocular distance in P. tertius is at least 2× higher than its post-ocular distance, while that of P. coreodes is always less than 2× [ 31 , 38 ]. Additionally, recent evidence reported the existence of hybrid inviability in controlled crosses between P. tertius and P. coreodes [ 38 ].…”

Revisiting the hybridization processes in the Triatoma brasiliensis complex (Hemiptera, Triatominae): Interspecific genomic compatibility point to a possible recent diversification of the species grouped in this monophyletic complex

“…The gonads morphology of at least two adult male hybrids F1 from each cross (Table 1) was analyzed using a Leica MZ APO stereoscope microscope with Motic Advanced 3.2 plus image analysis system to assess the presence of the phenomenon of gonadal dysgenesis (which can be uni or bilateral) [61] and, posteriorly, cytogenetic analysis with Lacto-Acetic Orcein (De Vaio et al [62], with modifications according to Alevi et al [14]) were performed on slides prepared with these gonads and examined using Jenaval light microscopy (Zeiss), coupled to the digital camera and the Axio Vision LE 4.8 image analyzer system (Copyright © 2006-2009 Carl Zeiss Imaging Solutions Gmb H) to assess the degree of pairing between homeologous chromosomes (as established by Mendonc ¸a et al [27]). Lastly, all data of the literature referring to experimental crossing studies in the T. brasiliensis complex were compiled (Table 2), with emphasis in the analysis of the presence/absence of pre-zygotic reproductive barrier.…”