Colour polymorphism in the sea snake Emydocephalus annulatus

Evolutionary theory suggests that polymorphic traits can be maintained within a single population only under specific conditions, such as negative frequency-dependent selection or heterozygote advantage. Non-venomous turtle-headed sea snakes (Emydocephalus annulatus) living in shallow bays near Noumea in New Caledonia exhibit three colour morphs: black, black-and-white banded, and an intermediate (grey-banded) morph that darkens with age. We recorded morph frequencies during 18 consecutive years of surveys, and found that the numbers of recruits (neonates plus immigrants) belonging to each morph increased in years when that morph was unusually rare in the population, and decreased when that morph was unusually common. Thus, morph frequencies are maintained by negative frequency-dependent selection. We interpret the situation as Batesian mimicry of highly venomous sea snakes (Aipysurus, Hydrophis, Laticauda) that occur in the same bays, and range in colour from black-and-white banded to grey-banded. Consistent with the idea that mimicry may protect snakes from attack by large fish and sea eagles, behavioural studies have shown that smaller fish species in these bays flee from banded snakes but attack black individuals. As predicted by theory, mimetic (banded) morphs are less common than the cryptically-coloured melanic morph.

Methods
Three adjacent populaions were surveyed annually, in January, using mark-recapture methods. The colour phase of every individual was scored into one of three categories. The analyis looks at how the relative numbers of snakes of eachcolour morph changed through time in each population.

进化论指出，多态性状仅能在特定条件下于单一种群中得以维持，例如负频率依赖选择（negative frequency-dependent selection）或杂合子优势（heterozygote advantage）。栖息于新喀里多尼亚努美阿附近浅海湾的无毒龟头海蛇（Emydocephalus annulatus）存在三种体色型：黑色型、黑白环纹型，以及随年龄加深的中间型（灰环纹型）。我们在连续18年的调查中记录了各体色型的频率，结果发现：当某一色型在种群中异常稀少时，该色型的补充个体（新生幼体+迁入个体）数量会增加；而当该色型在种群中异常常见时，其补充个体数量则会减少。由此可见，该种群的体色型频率由负频率依赖选择维持。

我们将这一现象归因于对同海湾内分布的剧毒海蛇（艾氏海蛇属Aipysurus、海蛇属Hydrophis、扁尾海蛇属Laticauda）的贝茨拟态（Batesian mimicry），这些剧毒海蛇的体色涵盖从黑白环纹到灰环纹的多种类型。与拟态可保护海蛇免遭大型鱼类及海雕攻击的假说一致，行为学研究表明：该海湾中的小型鱼类会躲避环纹型海蛇，却会攻击黑色型个体。正如理论所预测的那样，拟态型（环纹型）的出现频率低于具有隐蔽体色的黑色型。

研究方法
我们于每年1月使用标记重捕法（mark-recapture methods）对3个相邻种群开展调查。将每一个体的体色类型划分为上述三类之一。本分析旨在探究各体色型海蛇的相对数量在每个种群中随时间的变化趋势。