Complementary sex determination substantially increases extinction proneness of haplodiploid populations

Abstract

The role of genetic factors in extinction is firmly established for diploid organisms, but haplodiploids have been considered immune to genetic load impacts because deleterious alleles are readily purged in haploid males. However, we show that singlelocus complementary sex determination ancestral to the haplodiploid Hymenoptera (ants, bees, and wasps) imposes a substantial genetic load through homozygosity at the sex locus that results in the production of inviable or sterile diploid males. Using stochastic modeling, we have discovered that diploid male production (DMP) can initiate a rapid and previously uncharacterized extinction vortex. The extinction rate in haplodiploid populations with DMP is an order of magnitude greater than in its absence under realistic but conservative demographic parameter values. Furthermore, DMP alone can elevate the base extinction risk in haplodiploids by over an order of magnitude higher than that caused by inbreeding depression in threatened diploids. Thus, contrary to previous expectations, haplodiploids are more, rather than less, prone to extinction for genetic reasons. Our findings necessitate a fundamental shift in approaches to the conservation and population biology of these ecologically and economically crucial insects.diploid male production ͉ haplodiploidy ͉ Hymenoptera ͉ pollinator decline ͉ conservation genetics H aplodiploid insects such as ants, bees, and wasps are crucial components of terrestrial ecosystems, and their conservation is essential for economic as well as ecological reasons (1-4). Despite the obvious differences that result from their sexdetermining mechanism, the conservation genetics of haplodiploids has received very little attention (5) and has been ignored in conservation efforts (6, 7). Inbreeding depression in diploid organisms significantly increases extinction risk (8-11), but faster purging of recessive deleterious mutations in haploid males is believed to render haplodiploids relatively immune to its effects (12-14), theoretically reducing their intrinsic extinction risk, compared with diploids. However, single-locus complementary sex determination (sl-CSD), ancestral in the Hymenoptera, introduces an unusual source of genetic load in small populations (15): the production of inviable or effectively sterile diploid males (DMs) from fertilized eggs homozygous at the sexdetermining locus, csd (16-19) (Fig. 1).Large haplodiploid populations can maintain many csd alleles (commonly 9-20 alleles; ref. 15) and thus have low levels of DM production (DMP). However, drift in small populations reduces csd allelic richness and increases DMP (15). Several studies have documented low levels of csd allelic richness (Ͻ5 alleles) in both natural and introduced populations (20-24). Because female hymenopterans fertilize their eggs to produce daughters only, the production of DMs effectively increases female mortality, thus reducing the potential for population growth (25) (Fig. 1). Further, DMP also reduces the effective breeding size of haplodiploids, espe...

Orchid bees: a new assessment on the rarity of diploid males in populations of this group of Neotropical pollinators

“…Although, several recent studies have shown that 2N males are viable (Cowan and Stahlhut 2004;Elias et al 2009;Harpur et al 2013), they usually exhibit low fitness (Unruh and Messing 1993) and are thus considered very costly to populations of haplodiploid insects (Crozier 1977;Unruh and Messing 1993;Beye et al 2003;Heimpel and de Boer 2008;Zayed 2009;Harpur et al 2013). In addition, considering that for each diploid male produced a functional female ceases to be raised, diploid males inflict a significant cost on the reproductive success of their parents (Unruh and Messing 1993;Zayed and Packer 2005;Zayed 2009). …”

Diploid males of Scaptotrigona depilis are able to join reproductive aggregations (Apidae, Meliponini)

“…Simulation models have shown that extinction risks increase when diploid males are viable and can mate (Zayed and Packer 2005). This is expected because females mortality would increase over two generations, first in the diploid offspring that was supposed to be female but ends as an infertile diploid male, and secondly because the females that mate with diploid male would produce triploid daughters or only haploid males (Harpur et al 2013).…”

“…Most of the time they are unviable, infertile or lead to the production of infertile triploid broods (Heimpel and de Boer 2008). They also lead to the decrease of females in the population, since the diploid individuals were supposed to develop into females, increasing the extinction risks of the population (Zayed and Packer 2005).…”

Conservation genetics of bees: advances in the application of molecular tools to guide bee pollinator conservation

“…In bees and other haplodiploid insects with single locus complementary sex determination, the risk of inbreeding depression associated with the loss of genetic diversity is higher than in diploid organisms because sterile diploid males are produced if the sex determination locus is homozygous. Therefore, estimating levels of male diploidy can reveal genetic degradation at the population level and could assist in the identification of populations of conservation concern (Zayed and Packer 2005).…”

“…Population genetic studies can shed light on potential drivers of dispersal from inferred genetic structure (Jha 2015). At contemporary time scales, reduced genetic diversity in a population can increase the risk of inbreeding (Zayed and Packer 2005), and inbreeding depression can result in fitness declines, such as slower growth rates and lower reproductive rates (Whitehorn et al 2009). In bees and other haplodiploid insects with single locus complementary sex determination, the risk of inbreeding depression associated with the loss of genetic diversity is higher than in diploid organisms because sterile diploid males are produced if the sex determination locus is homozygous.…”