Hologenomic speciation: synergy between a male-killing bacterium and sex-linkage creates a ‘magic trait’ in a butterfly hybrid zone

Abstract

Danaus chrysippus (L.) in Africa comprises four substantially isolated semispecies that are migratory and hybridize on a seasonal basis throughout the eastern and central part of the continent. In the hybrid zone (but not elsewhere), the butterfly is commonly host to a male killing endosymbiotic bacterium, Spiroplasma sp., which principally infects one semispecies, Danaus chrysippus chrysippus in Kenya. A W-autosome mutation, inherited strictly matrilinearly, links B and C colour gene loci, which have thus gained sex-linkage in chrysippus. We have monitored variation in sex ratio and genotype at the A and C colour gene loci for two extended periods of 18 months (2004-5) and 12 months (2009-10) in adults reared from wild eggs laid on trap plants in Kasarani, near Nairobi, Kenya. Additionally, in 2009-10, all surviving adult butterflies were screened for Spiroplasma infection. The hybridizing Kasarani population is highly atypical in three respects, and has apparently been so for some 30 years: first, the sex ratio is permanently female-biased (as expected), although subject to seasonal fluctuation, being lowest (male/female) when D. c. chrysippus (cc) peaks and highest when Danaus chrysippus dorippus (CC) predominates; second, the population is invariably dominated by Cc heterozygotes of both sexes but especially females; and third, cc males are always scarce because they are systematically eliminated by male killing, whereas the CC genotype is male-biased. It is this imbalance of sex versus genotype that determines the massive departure from Hardy-Weinberg equilibrium in the population, in part because cc females have little choice but to pair with C-males. We suggest that: first, Cc hybrids of both sexes fail to disperse in the company of either parental semispecies; second, Spiroplasma positive females carrying the W-autosome mutation have a selective advantage over females that lack the translocation; third, the endoparasite and the translocation create a 'magic trait' linkage group that underlies hologenomic reproductive isolation between two emerging species, D. c. chrysippus and D. c. dorippus; and, fourth, that the predominance of males in dorippus suggests that individuals must be protected by a male-killing suppressor gene. By contrast to the C locus, Aa heterozygotes are in substantial and permanent deficit, suggesting either assortative mating between AA (chrysippus and dorippus) and aa (Danaus chrysippus alcippus), or heterozygote unfitness, or both.

Holes in the Hologenome: Why Host-Microbe Symbioses Are Not Holobionts

“…One appeal of the “hologenome” is that it provides a nifty term for referencing the host plus microbiome. This may account for its recent use in some host-microbiome papers ( 14 – 16 , 72 – 74 ), even when these microbial communities did not meet the narrow conditions necessary for a hologenome. The terms “holobiont” and “hologenome” elevate the host plus its microbiome to the status of an organism.…”

Whole-chromosome hitchhiking driven by a male-killing endosymbiont

“…What is particularly striking is that the presence of the neo-W coincides with infection by a maternally-inherited 'male killer' endosymbiont related to Spiroplasma ixodetis, which kills male offspring and leads to highly female-biased sex-ratios where infection is common [22][23][24]. The combination of neo-W and male killing is expected to dramatically alter the inheritance and evolution of the BC chromosome [22,25]: Infected females typically give rise to all-female broods who should always inherit the same colour patterning allele on their neo-W, along with the male-killer, while the other maternal allele is systematically eliminated in the dead sons ( Fig. 1B), forming a genetic sink for all colour pattern alleles not on the neo-W.…”

“…1B), forming a genetic sink for all colour pattern alleles not on the neo-W. It has been suggested that the restriction of male killing to females with the neo-W, and only in the region in which hybridisation occurs between subspecies, may not be a coincidence [19,22,[25][26][27]. However, the genomic underpinnings of this system -the genetic controllers of colour pattern, the source and spread of the neo-W, and its relationship with the male killer -have until now remained a mystery.…”

A neo-W chromosome in a tropical butterfly links colour pattern, male-killing, and speciation

“…We have previously found that the c -autosome of chrysippus females strictly segregates with the W chromosome within the hybrid zone and have, therefore, postulated that a W-autosomal fusion ( ) had occurred [ 18 – 20 ], physically linking the female determining W chromosome with the colour pattern locus C . Further, we have also found within the hybrid zone that chrysippus females and their transiens daughters are all infected with the male-killing Spiroplasma and thus produce all-female broods whereas, by contrast, dorippus females are largely uninfected by Spiroplasma and, therefore, continue to produce both males and females.…”