skip to main content


Title: Population Genetics of Reproductive Genes in Haplodiploid Species
Abstract Many animal species are haplodiploid: their fertilized eggs develop into diploid females and their unfertilized eggs develop into haploid males. The unique genetic features of haplodiploidy raise the prospect that these systems can be used to disentangle the population genetic consequences of haploid and diploid selection. To this end, sex-specific reproductive genes are of particular interest because, while they are shared within the same genome, they consistently experience selection in different ploidal environments. However, other features of these genes, including sex-specific expression and putative involvement in postcopulatory sexual selection, are potentially confounding factors because they may also impact the efficacy of selection asymmetrically between the sexes. Thus, to properly interpret evolutionary genomic patterns, it is necessary to generate a null expectation for the relative amount of polymorphism and divergence we expect to observe among sex-specific genes in haplodiploid species, given differences in ploidal environment, sex-limited expression, and their potential role in sexual selection. Here, we derive the theoretical expectation for the rate of evolution of sex-specific genes in haplodiploid species, under the assumption that they experience the same selective environment as genes expressed in both sexes. We find that the null expectation is that reproductive genes evolve more rapidly than constitutively expressed genes in haplodiploid genomes. However, despite the aforementioned differences, the null expectation does not differ between male- and female-specific reproductive genes, when assuming additivity. Our theoretical results provide an important baseline expectation that should be used in molecular evolution studies comparing rates of evolution among classes of genes in haplodiploid species.  more » « less
Award ID(s):
2143063
NSF-PAR ID:
10417846
Author(s) / Creator(s):
; ; ;
Editor(s):
Mank, Judith
Date Published:
Journal Name:
Genome Biology and Evolution
Volume:
14
Issue:
6
ISSN:
1759-6653
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. null (Ed.)
    Elevated rates of evolution in reproductive proteins are commonly observed in animal species, and are thought to be driven by the action of sexual selection and sexual conflict acting specifically on reproductive traits. Whether similar patterns are broadly observed in other biological groups is equivocal. Here, we examine patterns of protein divergence among wild tomato species ( Solanum section Lycopersicon ), to understand forces shaping the evolution of reproductive genes in this diverse, rapidly evolving plant clade. By comparing rates of molecular evolution among loci expressed in reproductive and non-reproductive tissues, our aims were to test if: (a) reproductive-specific loci evolve more rapidly, on average, than non-reproductive loci; (b) ‘male’-specific loci evolve at different rates than ‘female’-specific loci; (c) genes expressed exclusively in gametophytic (haploid) tissue evolve differently from genes expressed in sporophytic (diploid) tissue or in both tissue types; and (d) mating system variation (a potential proxy for the expected strength of sexual selection and/or sexual conflict) affects patterns of protein evolution. We observed elevated evolutionary rates in reproductive proteins. However, this pattern was most evident for female- rather than male-specific loci, both broadly and for individual loci inferred to be positively selected. These elevated rates might be facilitated by greater tissue-specificity of reproductive proteins, as faster rates were also associated with more narrow expression domains. In contrast, we found little evidence that evolutionary rates are consistently different in loci experiencing haploid selection (gametophytic-exclusive loci), or in lineages with quantitatively different mating systems. Overall while reproductive protein evolution is generally elevated in this diverse plant group, some specific patterns of evolution are more complex than those reported in other (largely animal) systems, and include a more prominent role for female-specific loci among adaptively evolving genes. 
    more » « less
  2. 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
  3. Abstract The prevalent mode of reproduction among ants is arrhenotokous parthenogenesis where unfertilized eggs give rise to haploid males and fertilized eggs develop into diploid females. Some ant species are capable of thelytokous parthenogenesis, a type of asexual reproduction where females develop from unfertilized diploid eggs. Thelytoky is well-documented in more than 20 ant species. Cytogenetic data are available for six species demonstrating that some thelytokous ant species are capable of producing males occasionally as well as maintaining their chromosome numbers and proper chromosome pairings. Mycocepurus smithii is a thelytokous fungus-growing ant species that inhabits large parts of Central and South America. Cytogenetic data are unavailable for M. smithii and male individuals were never documented for this species, although the presence of males is expected because genetic recombination was observed in a few sexually reproducing populations in Brazil and haploid sperm was documented from the spermathecae of M. smithii queens. This study aims at comparatively studying asexual and sexual populations of M. smithii using classical and molecular cytogenetic methods to test whether karyotype configuration is modified according to the mode of reproduction in M. smithii . Moreover, we report the discovery of M. smithii males from a sexually reproducing population in the Brazilian state Pará, diagnose the male of M. smithii , and morphologically characterize their spermatozoa. Karyotypic variation was observed within the asexual population (2n = 9, 10, or 11), whereas the chromosome number was fixed in the sexual population (2n = 14, n = 7). Identical karyotypes were maintained within individual M. smithii colonies and karyotype variation was only observed between colonies. In asexual individuals, the karyomorphs showed a decay of homologous chromosome pairs, especially in individuals with the karyomorph 2n = 11, which is potentially caused by relaxed natural selection on proper chromosome pairing. In contrast, females in the sexual population showed proper homologous chromosome pairings. In individuals of both asexual and sexual populations, we find that heterochromatin was localized in centromeric regions and on the short arms of the chromosomes, GC-rich regions were associated with heterochromatic regions, and 18S rDNA genes were located on the largest chromosome pair. This comparative cytogenetic analysis contributes to our understanding about the cytological mechanisms associated with thelytokous parthenogenesis in ants and suggests the decay of chromosome structure in the absence of meiosis and genetic recombination. 
    more » « less
  4. Abstract

    Maternal inheritance of mitochondria creates a sex‐specific selective sieve through which mitochondrial mutations harmful to males but not females accumulate and contribute to sexual differences in longevity and disease susceptibility. Because eggs and sperm are under disruptive selection, sperm are predicted to be particularly vulnerable to the genetic load generated by maternal inheritance, yet evidence for mitochondrial involvement in male fertility is limited and controversial. Here, we exploit the coexistence of two divergent mitochondrial haplogroups (A and B2) in a Neotropical arachnid to investigate the role of mitochondria in sperm competition. DNA profiling demonstrated that B2‐carrying males sired more than three times as many offspring in sperm competition experiments than A males, and this B2 competitive advantage cannot be explained by female mitochondrial haplogroup or male nuclear genetic background. RNA‐Seq of testicular tissues implicates differential expression of mitochondrial oxidative phosphorylation (OXPHOS) genes in the B2 competitive advantage, including a 22‐fold upregulation ofatp8in B2 males. Previous comparative genomic analyses have revealed functionally significant amino acid substitutions in differentially expressed genes, indicating that the mitochondrial haplogroups differ not only in expression but also in DNA sequence and protein functioning. However, mitochondrial haplogroup had no effect on sperm number or sperm viability, and, when females were mated to a single male, neither male haplogroup, female haplogroup nor the interaction between male/female haplogroup significantly affected female reproductive success. Our findings therefore suggest that mitochondrial effects on male reproduction may often go undetected in noncompetitive contexts and may prove more important in nature than is currently appreciated.

     
    more » « less
  5. Abstract

    Evaluating the fitness of hybrids can provide important insights into genetic differences between species or diverging populations. We focused on surface- and cave-ecotypes of the widespread Atlantic molly Poecilia mexicana and raised F1 hybrids of reciprocal crosses to sexual maturity in a common-garden experiment. Hybrids were reared in a fully factorial 2 × 2 design consisting of lighting (light vs. darkness) and resource availability (high vs. low food). We quantified survival, ability to realize their full reproductive potential (i.e., completed maturation for males and 3 consecutive births for females) and essential life-history traits. Compared to the performance of pure cave and surface fish from a previous experiment, F1s had the highest death rate and the lowest proportion of fish that reached their full reproductive potential. We also uncovered an intriguing pattern of sex-specific phenotype expression, because male hybrids expressed cave molly life histories, while female hybrids expressed surface molly life histories. Our results provide evidence for strong selection against hybrids in the cave molly system, but also suggest a complex pattern of sex-specific (opposing) dominance, with certain surface molly genes being dominant in female hybrids and certain cave molly genes being dominant in male hybrids.

     
    more » « less