Entelegyne spiders rarely show fusions yielding neo-Y chromosomes, which M. J. D. White attributed to a constraint in spiders, namely their proximal chiasma localization acting to upset meiotic segregation in males with fusions. Of the 75 taxa of Habronattus and outgroups studied, 47 have X1X20 sex chromosomes in males, 10 have X1X2Y, 15 have X1X2X3Y, 2 have X0, and one has both X1X20 and X1X2X3Y. Chromosome numbers and behavior suggest neo-Ys formed by an autosome-X fusion to make X1X2Y, with a second fusion to an autosome to make X1X2X3Y. Phylogeny shows at least 8-15 gains (or possibly some losses) of neo-Y (i.e. X-autosome fusions), a remarkable number for such a small clade. In contrast to the many X-autosome fusions, at most one autosome-autosome fusion is indicated. Origins of neo-Y are correlated significantly with distal localization of chiasmata, supporting White’s hypothesis that evolution of neo-Y systems is facilitated by looser pairing (distal chiasmata) at meiosis. However, an alternative (or contributing) explanation for the correlation is that X-autosome fusions were selected to permit isolation of male-favored alleles to the neo-Y chromosome, aided by distal chiasmata limiting recombination. This intralocus sexual conflict hypothesis could explain both the many X-autosome fusions, and the stunning complexity of male Habronattus courtship displays.