The Y-chromosome and mitochondria (containing mtDNA) appear entirely dissimilar, the former being a sex chromosome found in the nucleus and the latter an organelle with thousands of copies in the cytoplasm. However, both experience uniparental inheritance, with Y-chromosomes being patrilineal and mitochondria matrilineal. This leads to various other similarities including haploidy, high mutation rates, and limited or lack of genetic recombination. Moreover, the low number of protein-coding genes contained on both led to the belief that neither contributes significantly to the adaptive evolution of complex traits. However, recent studies show the Y-chromosome and mitochondria both influence roughly 10% of male transcripts, greatly increasing their evolutionary reach. The nature of the mitochondria's influence is clear – maternal inheritance leads to the accumulation of male-deleterious mutations that negatively impact autosomal and X-linked transcripts (termed mother's curse). However, the nature of the Y-linked variation is less clear, but may impact the manifestation of mother's curse, the evolution of sexual dimorphism, or even act as a constraint on adaptive evolution. In Chapter 2, we explore the potential for Y-chromosomes to influence sexual dimorphism by examining the nature of Y-linked genetic variance. If this variance is additive, it may facilitate the evolution of sexual dimorphism by allowing male traits to be shaped independently of female traits despite males sharing a genome with females. However, if this variance is epistatic, it may slow population level responses to strong selective pressures such as climate change or novel diseases. To date, previous works suggest that Y-linked variation is predominately epistatic. To address our objective, we compare fruit fly populations with and without Y-linked variance and measure the heritability of male and female morphological traits. Surprisingly, we find more heritable variance in populations with Y-linked variance, suggestive of Y-linked additivity. In Chapter 3, we examine whether Y-linked variation can counteract mother's curse. Theoretically, compensatory mutations could evolve on the autosomes, X-chromosome, or Y-chromosome. However, Ys appear best suited to host these mutations as there can be no counter-selection from females due to the Y's uniparental inheritance. To test this, we placed coevolved and non-coevolved Ys and mitochondria into an isogenic background that shared no coevolutionary history with either genetic element. We find that the Y-chromosome has the potential to compensate for mother's curse for at least one trait, male longevity. In Chapter 4, we address a potential limitation in our previous test for Y-linked compensation in Chapter 3: the non-coevolved nuclear background. Theoretically, Ys may compensate for mitochondrial mutations by interacting with the autosomes. Thus, having a coevolved Y and autosomal background may be critical to compensation. To this end, we repeated our experiments from Chapter 3 with the inclusion of a coevolved nuclear genome. We again find Y-chromosomal compensation for mother's curse for longevity, but only when coevolved autosomes are used. This suggests that using non-coevolved backgrounds (as all previous studies have done) may be unreliable and create misleading results.
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Doctor of Philosophy (Ph.D.)
College of Sciences
Integrative Conservation Biology; Integrative Biology
Length of Campus-only Access
Doctoral Dissertation (Open Access)
Nielsen, Tobias, "The Y-Chromosome's Role in Sexually Dimorphic Evolution and Mother's Curse Compensation" (2022). Electronic Theses and Dissertations, 2020-. 1720.