Intraspecific chromosome polymorphisms can lead to reproductive isolation and speciation: an example in red brocket deer (Mazama americana)

Abstract

The red brocket (Mazama americana) is a South American deer with a wide geographical distribution that presents different chromosomal variants depending on their location. At least six different cytotypes belonging to two distinct evolutionary lineages have been described. This study aimed to verify the existence of postzygotic reproductive isolation between cytotypes of M. americana by comparative evaluation of pure and hybrid males. Seven 18-month-old bucks were submitted to seminal collection and evaluation and testicle histological evaluations. The pure males showed normal parameters for sperm quality and testicular histology. Hybrids from the same evolutionary lineage (≤3 chromosomes different from the progenitors) showed similar results to pure males, except for the reduced ratio of round spermatids to pachytene spermatocytes. Hybrids between cytotypes of different evolutionary lineages (≥10 chromosomes different from progenitors) presented azoospermia and evidence of testicular degeneration. Despite the striking morphological similarities, we can conclude that populations with more distinct karyotypes possess an effective reproductive barrier; moreover, there is evidence that reproductive isolation mechanisms exist between some closer karyotypes, corroborating the hypothesis that M. americana is best characterized as a superspecies. Thus, the future description of several new species for this taxon is expected, since the tendency is to establish efficient mechanisms of postzygotic reproductive isolation, preventing the introgression and fusion of genomes from different populations through chromosome variation.

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“…Lineages included in this study may be considered as different species, since high levels of molecular and cytogenetic differentiation have been shown between them (Duarte et al, 2008). Similarly, from a reproductive point of view, the existence of well-established post-zygotic isolation between the most distant karyotype lineages has been also proved (Cursino et al, 2014;Salviano et al, 2017). All these results along with the findings of this study on the absence of clear pre-zygotic barriers among cytotypes have important implications for the conservation of these species.…”

“…The analysis of the cytogenetic evolution has recently shown the existence of two karyotypic lineages that evolved from a common ancestor by chromosomal rearrangements: Lineage A, which includes the Rondônia and Juína karyotypes; and Lineage B, which includes the Jarí, Carajás, Santarém, and Paraná karyotypes (Abril et al, 2010). Both lineages are also well differentiated at the level of mtDNA (Abril et al, 2010) and maintain reproductive isolation, with hybrids showing sterility or subfertility (Aquino et al, 2013;Cursino et al, 2014;Salviano et al, 2017). All these results clearly point to the existence of at least two separate species within the current Mazama americana specific nomination, which need to be formally described, and probably a deeper investigation could reveal further subdivisions under an ongoing process of rapid sympatric speciation based on chromosomal rearrangements (Abril et al, 2010).…”

Designation of a neotype for Mazama americana (Artiodactyla, Cervidae) reveals a cryptic new complex of brocket deer species

“…This polymorphism would suggest a rapid speciation process driven by chromosomal rearrangements, with a diploid number of chromosomes ranging between 42 and 52, considered within six geographically established cytotypes (Duarte et al 2008;Abril et al 2010). As a result of this chromosomal variation, reproductive isolation has occurred in animals due to sterility problems caused by chromosomal meiosis pairing between different chromosomal lineages (Aquino et al 2013;Cursino et al 2014;Salviano et al 2017). The populations in south-central South America are reproductively isolated from the Amazonian populations, being different species (Cursino et al 2014;Salviano et al 2017), that until now have not been described or nominated.…”

“…As a result of this chromosomal variation, reproductive isolation has occurred in animals due to sterility problems caused by chromosomal meiosis pairing between different chromosomal lineages (Aquino et al 2013;Cursino et al 2014;Salviano et al 2017). The populations in south-central South America are reproductively isolated from the Amazonian populations, being different species (Cursino et al 2014;Salviano et al 2017), that until now have not been described or nominated.…”

Intrapopulation Chromosomal Polymorphism in <b><i>Mazama gouazoubira</i></b> (Cetartiodactyla; Cervidae): The Emergence of a New Species?

“…However, heterozygotes for a single centric fusion generally form trivalents in meiosis, causing minimal problems in reproduction [Baker and Bickham, 1986], as observed in a meiotic study performed on M. americana [Aquino et al, 2013]. However, Cursino et al [2014] and Salviano et al [2017] verified that hybrids of different M. americana cytotypes possess a mechanism of post-zygotic reproductive isolation that involves subfertility or infertility, demonstrating reproductive isolation with the accumulation of chromosomal rearrangements. When accumulated fixation of several centric fusions occurs, reproductive isolation is increasingly likely due to gamete incompatibility [Dobigny et al, 2002].…”