Gene-Expression Changes Caused by Inbreeding Protect Against Inbreeding Depression in Drosophila

Abstract

We present a transcriptomic analysis aimed at investigating whether the changes in gene expression that occur under inbreeding generally reduce or enhance inbreeding depression. Discerning between these two alternatives can be addressed only when both changes in expression due to inbreeding and to inbreeding depression are estimated simultaneously. We used Affymetrix 2.0 arrays to study the changes in gene expression associated with both inbreeding and inbreeding depression for fitness in four sets of inbred sublines of Drosophila melanogaster. We found that for most genes showing changes in expression associated with inbreeding, the least depressed sublines were those showing the largest departures in expression from that of the outbred control. This suggests a pattern consistent with a protective role of expression changes against inbreeding effects, and would reveal a new dimension of the transcriptomics of inbreeding. The variation in depression observed could then be due not only to the genetic damages primarily originating that depression, but also possibly to differences in the ability to carry out the appropriate adjustments in gene expression to cope with the inbreeding. We also found that these expression changes with a putative protective role against inbreeding effects show a clear specificity on RNA synthesis and splicing and energy derivation functions. INBREEDING depression, the reduction in fitness observed in the progeny of genetically related individuals, plays a key role in population biology, affecting processes as diverse as the management of livestock and endangered wild species (Keller and Waller 2002;Koenig and Simianer 2006), the evolution of mating systems (Kelly 2005), and the dispersal strategies (Motro 1991;Gandon 1999). The population genetics of this depression is well understood (Lynch 1991;Charlesworth and Charlesworth 1999;Charlesworth and Willis 2009), but the genomic details about the mechanisms causing it are just starting to be unveiled (Paige 2010). In particular, it would be important to determine the relationship between gene regulation and inbreeding, as regulatory variation underlies much of phenotypic diversity (Wilson et al. 1974;Carroll 2005;Ranz and Machado 2006). Evidence has been provided for significant intraspecific variation in transcript abundance for a large fraction of the genome (Primig et al. 2000;Sandberg et al. 2000) and to show that much of such variation is heritable (Cavalieri et al. 2000;Karp et al. 2000;Jin et al. 2001), suggesting that regulatory variation is likely the main mediator of phenotypic divergence in evolution (King and Wilson 1975;Wray et al. 2003;Hoekstra and Coyne 2007). Therefore, genetic correlations between expression phenotypes and organismal phenotypes point to the molecular pathways that underlie the organismal phenotypes (Rockman and Kruglyak 2006). Thus, an understanding of the molecular basis of inbreeding depression requires knowledge of variation at the whole-genome level (Ayroles et al. 2009).Using whole-genome cD...

Inbreeding interferes with the heat-shock response

“…Recent studies showed that several pathways may be upregulated in inbred as compared with outbred Drosophila individuals, whereas others, though less commonly occurring, are downregulated (Kristensen et al, , 2006Pedersen et al, 2005;García et al, 2012). Similarly, Ayroles et al (2009) showed that inbreeding depression results in an overexpression of many genes associated with metabolism, stress or defence mechanisms.…”

Candidate Transcriptomic Sources of Inbreeding Depression in Drosophila melanogaster

“…The biological material used in this work is described in [19], where a detailed description of the experimental design and main analytical tools employed can be found. Briefly, the base population was founded in November 2006 from a large sample (>1000 females) collected in a wine cellar close to Vigo (Galicia, NW Spain).…”

“…Three replicates of the outbred control were also randomly chosen for analysis. For each sample, pools of 30 males from each selected inbred subline and from the outbred controls were used for total RNA extraction and hybridization with the array as described in [19]. We only analysed gene expressions in males to avoid the source of additional experimental variance associated to post-mating gene expression changes in females [32], or to different stages of egg development in pregnant females [33].…”

“…Again, many genes changed their expression between depression levels and those related with basic metabolism, stress and defence responses were overrepresented. In a previous paper [19] (see also [20]), we have presented the results of a new analysis where both inbreeding and inbreeding depression effects on gene expression are analysed. As in previous studies, we found that inbreeding caused large-scale changes in gene expression.…”

Are transcriptional responses to inbreeding a functional response to alleviate inbreeding depression?

“…1 In recent times, however, the advent of large-scale platforms to monitor [2][3][4] We made a gene expression analysis of inbreeding in Drosophila melanogaster males using the Affymetrix Drosophila Genechip Array 2.0 and aimed to distinguish the changes that alleviate the depression from those that generate it. 5 We started with four pairs (lines) of individuals and founded 55 full-sib mating inbred sublines with each. In generation eight, the sublines showed a great variation in pupa productivity (and thus inbreeding depression), despite having the same genealogical inbreeding coefficient (around 0.7).…”