Abstract The role of hybridization as a formative process in evolution has received much attention in the past few decades. A particularly fascinating outcome of hybrid speciation is the formation of asexual hybrid species. The Amazon molly (Poecilia formosa) is such a hybrid and originated from aP. mexicanamother and aP. latipinnafather. Consequently, a heterospecific mating must have occurred leading to the Amazon molly, indicating a breakdown of any potential prezygotic isolation between parental species. Here we studied the female mate preferences of extantP. mexicanaandP. latipinnafrom several populations using standard binary choice tests with males of both sexual species that were matched for size.Poecilia mexicanaandP. latipinnacan be crossed in the lab, however, the offspring are not asexual, but sexual F1s. In our study, we generated F1s and tested their mating preferences with sexual males of bothP. mexicanaandP. latipinnaagainst F1males. Overall, our results show that in extantP. mexicanaandP. latipinnano female preference for conspecific males was detectable. Consequently, heterospecific matings are possible and not hindered by any apparent behavioral prezygotic isolation. If female preferences in these species were comparable around the time the Amazon molly originated as a hybrid species ca. 100,000 years ago, matings leading to hybrids would be very likely. F1females also have no discernable mating preferences for either sexual males or F1males. Such lack of prezygotic behavioral isolation could potentially lead to F2individuals, backcrosses, and introgression.
more »
« less
A mitochondrial genetic divergence proxy predicts the reproductive compatibility of mammalian hybrids
Numerous pairs of evolutionarily divergent mammalian species have been shown to produce hybrid offspring. In some cases, F 1 hybrids are able to produce F 2 s through matings with F 1 s. In other instances, the hybrids are only able to produce offspring themselves through backcrosses with a parent species owing to unisexual sterility (Haldane's Rule). Here, we explicitly tested whether genetic distance, computed from mitochondrial and nuclear genes, can be used as a proxy to predict the relative fertility of the hybrid offspring resulting from matings between species of terrestrial mammals. We assessed the proxy's predictive power using a well-characterized felid hybrid system, and applied it to modern and ancient hominins. Our results revealed a small overlap in mitochondrial genetic distance values that distinguish species pairs whose calculated distances fall within two categories: those whose hybrid offspring follow Haldane's Rule, and those whose hybrid F 1 offspring can produce F 2 s. The strong correlation between genetic distance and hybrid fertility demonstrated here suggests that this proxy can be employed to predict whether the hybrid offspring of two mammalian species will follow Haldane's Rule.
more »
« less
- Award ID(s):
- 1753760
- PAR ID:
- 10161049
- Date Published:
- Journal Name:
- Proceedings of the Royal Society B: Biological Sciences
- Volume:
- 287
- Issue:
- 1928
- ISSN:
- 0962-8452
- Page Range / eLocation ID:
- 20200690
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Haldane’s rule—a pattern in which hybrid sterility or inviability is observed in the heterogametic sex of an interspecific cross—is one of the most widely obeyed rules in nature. Because inheritance patterns are similar for sex chromosomes and haplodiploid genomes, Haldane’s rule may apply to haplodiploid taxa, predicting that haploid male hybrids will evolve sterility or inviability before diploid female hybrids. However, there are several genetic and evolutionary mechanisms that may reduce the tendency of haplodiploids to obey Haldane’s rule. Currently, there are insufficient data from haplodiploids to determine how frequently they adhere to Haldane’s rule. To help fill this gap, we crossed a pair of haplodiploid hymenopteran species (Neodiprion lecontei and Neodiprion pinetum) and evaluated the viability and fertility of female and male hybrids. Despite considerable divergence, we found no evidence of reduced fertility in hybrids of either sex, consistent with the hypothesis that hybrid sterility evolves slowly in haplodiploids. For viability, we found a pattern opposite of Haldane’s rule: hybrid females, but not males, had reduced viability. This reduction was most pronounced in one direction of the cross, possibly due to a cytoplasmic-nuclear incompatibility. We also found evidence of extrinsic postzygotic isolation in hybrids of both sexes, raising the possibility that this form or reproductive isolation tends to emerge early in speciation in host-specialized insects. Our work emphasizes the need for more studies on reproductive isolation in haplodiploids, which are abundant in nature, but under-represented in the speciation literature.more » « less
-
Barbash, D A (Ed.)Abstract Embryonic development in mammals is highly sensitive to changes in gene expression within the placenta. The placenta is also highly enriched for genes showing parent-of-origin or imprinted expression, which is predicted to evolve rapidly in response to parental conflict. However, little is known about the evolution of placental gene expression, or if divergence of placental gene expression plays an important role in mammalian speciation. We used crosses between two species of dwarf hamsters (Phodopus sungorus and Phodopus campbelli) to examine the genetic and regulatory underpinnings of severe placental overgrowth in their hybrids. Using quantitative genetic mapping and mitochondrial substitution lines, we show that overgrowth of hybrid placentas was primarily caused by genetic differences on the maternally inherited P. sungorus X chromosome. Mitochondrial interactions did not contribute to abnormal hybrid placental development, and there was only weak correspondence between placental disruption and embryonic growth. Genome-wide analyses of placental transcriptomes from the parental species and first- and second-generation hybrids revealed a central group of co-expressed X-linked and autosomal genes that were highly enriched for maternally biased expression. Expression of this gene network was strongly correlated with placental size and showed widespread misexpression dependent on epistatic interactions with X-linked hybrid incompatibilities. Collectively, our results indicate that the X chromosome is likely to play a prominent role in the evolution of placental gene expression and the accumulation of hybrid developmental barriers between mammalian species.more » « less
-
Hybrids account for nearly all commercially planted varieties of maize and many other crop plants because crosses between inbred lines of these species produce first-generation [F1] offspring that greatly outperform their parents. The mechanisms underlying this phenomenon, called heterosis or hybrid vigor, are not well understood despite over a century of intensive research. The leading hypotheses—which focus on quantitative genetic mechanisms (dominance, overdominance, and epistasis) and molecular mechanisms (gene dosage and transcriptional regulation)—have been able to explain some but not all of the observed patterns of heterosis. Abiotic stressors are known to impact the expression of heterosis; however, the potential role of microbes in heterosis has largely been ignored. Here, we show that heterosis of root biomass and other traits in maize is strongly dependent on the belowground microbial environment. We found that, in some cases, inbred lines perform as well by these criteria as their F1offspring under sterile conditions but that heterosis can be restored by inoculation with a simple community of seven bacterial strains. We observed the same pattern for seedlings inoculated with autoclaved versus live soil slurries in a growth chamber and for plants grown in steamed or fumigated versus untreated soil in the field. In a different field site, however, soil steaming increased rather than decreased heterosis, indicating that the direction of the effect depends on community composition, environment, or both. Together, our results demonstrate an ecological phenomenon whereby soil microbes differentially impact the early growth of inbred and hybrid maize.more » « less
-
Abstract As populations differentiate across geographic or host‐association barriers, interpopulation fertility is often a measure of the extent of incipient speciation. The bed bug,Cimex lectulariusL., was recently found to form two host‐associated lineages within Europe: one found with humans (human‐associated, HA) and the other found with bats (bat‐associated, BA). No unequivocal evidence of contemporary gene flow between these lineages has been found; however, it is unclear whether this is due to an inability to produce viable “hybrid” offspring. To address this question and determine the extent of compatibility between host‐associated lineages, we set up mating crosses among populations of bed bugs based on both their host association (human—HA vs. bat—BA) and geographic origin (North America vs. Europe). Within‐population fecundity was significantly higher for all HA populations (>1.7 eggs/day) than for BA populations (<1 egg/day). However, all within‐population crosses, regardless of host association, had >92% egg hatch rates. Contrary to previous reports, in all interlineage crosses, successful matings occurred, fertile eggs were oviposited, and the F1“hybrid” generation was found to be reproductively viable. In addition, we evaluated interpopulation genetic variation inWolbachiaamong host‐associated lineages. We did not find any clear patterns related to host association, nor did we observe a homogenization ofWolbachialineages across populations that might explain a breakdown of reproductive incompatibility. These results indicate that while the HA and BA populations ofC. lectulariusrepresent genetically differentiated host‐associated lineages, possibly undergoing sympatric speciation, this is in its incipient stage as they remain reproductively compatible. Other behavioral, physiological, and/or ecological factors likely maintain host‐associated differentiation.more » « less
An official website of the United States government

