Loss of recombination between sex chromosomes often depletes Y chromosomes of functional content and genetic variation, which might limit their potential to generate adaptive diversity. Males of the freshwater fish Poecilia parae occur as one of five discrete morphs, all of which shoal together in natural populations where morph frequency has been stable for over 50 years. Each morph utilizes a different complex reproductive strategy, and morphs differ dramatically in color, body size, and mating behavior.Morph phenotype is passed perfectly from father to son, indicating there are five Y haplotypes segregating in the species, which encode the complex male morph characteristics. Here, we examine Y diversity in natural populations of P. parae. Using linked-read sequencing on multiple P. parae females and males of all five morphs, we find that the genetic architecture of the male morphs evolved on the Y chromosome after recombination suppression had occurred with the X. Comparing Y chromosomes between each of the morphs, we show that although the Ys of the three minor morphs that differ in color are highly similar, there are substantial amounts of unique genetic material and divergence between the Ys of the three major morphs that differ in reproductive strategy, body size and mating behavior.Altogether, our results suggest that the Y chromosome is able to overcome the constraints of recombination loss to generate extreme diversity, resulting in five discrete Y chromosomes that control complex reproductive strategies. morphs. Most importantly, multigeneration pedigrees show that morph phenotype is always passed perfectly from father to son 13 , indicating the five P. parae morphs are controlled by five different Y chromosomes. This system therefore offers the potential for a unique insight into the adaptive potential of Y chromosomes, and the role of these regions of the genome in male phenotypes. Y chromosomes are formed once recombination with the X is halted 1 , and the loss of recombination on the Y leads to a complex cascade of non-adaptive processes that lead to the rapid buildup of heterochromatin and loss of gene activity [21][22][23] . However, the process of Y degeneration is not linear 24 , and although poecilid species closely related to P. parae share the same homologous sex chromosome as Poecilia reticulata 25 (guppies), the extent of Y chromosome degeneration differs markedly across the clade. Although the Y chromosome in P. reticulata and Poecilia wingei contains only a small area of limited degeneration [25][26][27][28] , the entirety of the Y chromosome of Poecilia picta is highly degenerate 25 . P. parae is a sister species of P. picta (diverging ~14.8 mya 29 ), however P. picta males are markedly different from P. parae and do not resemble any of the five P. parae morphs 18,20,[30][31][32] , suggesting remarkable diversity was generated on the P. parae Y chromosome after recombination was halted with the X chromosome. Work on model systems has indeed shown Y chromosomes can accumulate new genetic...