Complex Genotype by Environment interactions and changing genetic architectures across thermal environments in the Australian field cricket, Teleogryllus oceanicus

Abstract

BackgroundBiologists studying adaptation under sexual selection have spent considerable effort assessing the relative importance of two groups of models, which hinge on the idea that females gain indirect benefits via mate discrimination. These are the good genes and genetic compatibility models. Quantitative genetic studies have advanced our understanding of these models by enabling assessment of whether the genetic architectures underlying focal phenotypes are congruent with either model. In this context, good genes models require underlying additive genetic variance, while compatibility models require non-additive variance. Currently, we know very little about how the expression of genotypes comprised of distinct parental haplotypes, or how levels and types of genetic variance underlying key phenotypes, change across environments. Such knowledge is important, however, because genotype-environment interactions can have major implications on the potential for evolutionary responses to selection.ResultsWe used a full diallel breeding design to screen for complex genotype-environment interactions, and genetic architectures underlying key morphological traits, across two thermal environments (the lab standard 27°C, and the cooler 23°C) in the Australian field cricket, Teleogryllus oceanicus. In males, complex three-way interactions between sire and dam parental haplotypes and the rearing environment accounted for up to 23 per cent of the scaled phenotypic variance in the traits we measured (body mass, pronotum width and testes mass), and each trait harboured significant additive genetic variance in the standard temperature (27°C) only. In females, these three-way interactions were less important, with interactions between the paternal haplotype and rearing environment accounting for about ten per cent of the phenotypic variance (in body mass, pronotum width and ovary mass). Of the female traits measured, only ovary mass for crickets reared at the cooler temperature (23°C), exhibited significant levels of additive genetic variance.ConclusionsOur results show that the genetics underlying phenotypic expression can be complex, context-dependent and different in each of the sexes. We discuss the implications of these results, particularly in terms of the evolutionary processes that hinge on good and compatible genes models.

The more pieces, the better the puzzle: sperm concentration increases gametic compatibility

“…Our results suggest that compatibility effects in particular need to be considered in context of the environment they are measured (see also Nystrand et al. ; Eads et al. ; Lymbery and Evans ).…”

“…The relative importance of good and compatible gene effects (or compatibility driven by polyspermy risk) may not be consistent across these environments, with only a few studies to date having assessed the influence of the environment on the relative importance of good gene and genetic compatibility effects (Nystrand et al. ; Eads et al. ; Lymbery and Evans ).…”

“…Additionally, several quantitative‐genetic studies are required to determine how the relative importance of good genes and compatible genes benefits change across a range of other potentially relevant environmental gradients such as number of competing males, mating order, differential maternal effects, pH, and temperature (Nystrand et al. ; Eads et al. ; Lymbery and Evans ).…”

The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change?

“…For instance, thermal stress altered the expression of nonadditive genetic variance for morphological traits in the field cricket, Teleogryllus oceanicus (Nystrand, Dowling, & Simmons, 2011) and for larval hatching success in the sea urchin, Heliocidaris erythrogramma (Lymbery & Evans, 2013). Conversely, Foo, Dworjanyn, Poore, and Byrne (2012) found no effects of temperature or pH on nonadditive genetic effects on embryonic development in the sea urchin, Centrostephanus rodgersii , nor were maternal effects on development sensitive to CO 2 in another sea urchin, Strongylocentrotus franciscanus , or the mussel, Mytilus trossulus (Sunday, Crim, Harley, & Hart, 2011).…”

The effects of a bacterial challenge on reproductive success of fruit flies evolved under low or high sexual selection

“…Sex‐specificity in the degree to which costs of sexual selection are manifested across environments could have an underrated influence on shaping trajectories of trait evolution (Ingleby, Hunt, & Hosken, ). Natural populations are constantly exposed to heterogeneous and changing environments (Anderson, Wagner, Rushworth, Prasad, & Mitchell‐Olds, ; Candolin & Heuschele, ), and there are plenty of examples to support widespread gene by environmental effects in a range of phenotypic traits (Bashir‐Tanoli & Tinsley, ; Fanara, Folguera, Iriarte, Mensch, & Hasson, ; Howick & Lazzaro, ; Lazzaro, Flores, Lorigan, & Yourth, ; Nystrand, Dowling, & Simmons, ). Thus, there is a clear need for more research exploring evolutionary trajectories of populations under divergent levels of sexual interaction across a range of environmental contexts.…”