Does seasonality explain the evolution and maintenance of delayed implantation in the family Mustelidae (Mammalia: Carnivora)?

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Abstract

Understanding the evolutionary pressures that may have led to the development and retention of delayed implantation in mammals remains an enigmatic puzzle for evolutionary ecologists. Recent studies suggest a strong role of environmental conditions but other attributes of species, notably body size and life history traits, may obscure primary mechanisms. Following the recommendation of Lindenfors et al., we examined environmental correlates related to the evolution of delayed implantation and its subsequent maintenance or loss in the family Mustelidae (Mammalia: Carnivora). We focused on the Mustelidae because evolution and subsequent loss of delayed implantation occurred most commonly within this group. Data on 34 species of mustelids from around the world suggest that delayed implantation may have evolved when optimal times for mating and birthing are separated by more than a gestation period, characteristic of environments with long winters that reduce the opportunities to find mates. Environmental characteristics (seasonality, temperature, snow, latitude, and primary productivity) were highly intercorrelated but seasonality was the best predictor of the evolution or loss of delayed implantation via population traits. Here, structural equations on phylogenetic independent contrasts revealed that high seasonality was correlated with low population density and large individual home range size, which in turn was correlated with presence/absence of delayed implantation. We argue that the evolution of delayed implantation provides the reproductive means to mate during the season (summer) with the greatest prospects for females to ‘choose’ mates when living in high-latitude seasonal environments that generally reduce these opportunities (i.e. low population density and large ranges). Body mass of female mustelids did not differ between species with and without delayed implantation, refuting the hypothesis that loss of delayed implantation is an evolutionary by-product of evolving to smaller size. We conclude that understanding the environmental selection pressures responsible for the evolution of life history traits related to density and spacing behaviour allows for a more complete picture of the evolution and subsequent loss of delayed implantation.

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